Growth, maturation and survival of epiphytic ...

Hietz, Ausserer, Schindler: Growth of epiphytic bromeliads

Growth, maturation and survival of epiphytic bromeliads in a Mexican humid montane forest

Running title: Growth of epiphytic bromeliads

Keywords: Catopsis, epiphytes, growth, life history, population dynamics, Tillandsia, tropical montane forest

Peter Hietz*, Juliska Ausserer, Gudrun Schindler Institute of Botany, University of Agricultural Sciences, Gregor-Mendel Str. 33, A-1180 Vienna, Austria

* corresponding author: Institute of Botany, University of Agricultural Sciences, Gregor-Mendel Str. 33, A-1180 Vienna, Austria tel: +43-1-47654-3154, fax: +43-1-47654-4504, email: [email protected]

running headline: Growth of epiphytic bromeliads

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Abstract Growth and survival of plants of eight species of epiphytic bromeliads were studied over a period of 5 y in a humid montane forest in eastern Mexico using repeated photographs of branches. Growth was calculated from annual size increment and used to predict the time taken to reach fertility. Most intermediate-sized plants grew at a rate of 2 - 3 cm y-1, with the exception of Tillandsia deppeana, which does not invest in offshoots and grew about twice as fast. Tillandsia deppeana and two Catopsis spp. were predicted to become fertile after 11 and 9 y, respectively, T. multicaulis and T. punctulata after 13 y and T. juncea after 18 y. Individuals growing closer to the tree top tended to grow slightly faster. Relative growth rate calculated as biomass increase of the leading shoot was highest in T. deppeana and lowest in T. juncea. These differences are related to the proportion of biomass invested in offshoots, which are most numerous in T. juncea and mostly absent in T. deppeana. Fast maturation is particularly important for species growing on small and exposed branches, which experience higher mortalities caused by the breakage of their supporting branches.

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INTRODUCTION Vascular epiphytes are a conspicuous and characteristic element of tropical moist forests. Despite their often lush abundance, epiphytes supposedly grow slowly, mainly because water and nutrients occur in short and irregular supply in canopy habitats (Benzing 1990). Low rates of photosynthesis observed in epiphytes in the field accord with this assumption (Martin 1994, Stuntz & Zotz 2000), but direct and long-term observations of growth are few. Growth rates over a range of sizes are reported only for the bromeliad Tillandsia pauciflora (Benzing 1981, 1990) and the orchid Encyclia tampensis (Larson 1992) in Florida, and for the orchid Dimerandra emarginata in Panama (Zotz 1995, Zotz 1998). These three species were estimated to require at least 810, 15, and 6-10 y, respectively, to reach maturity. In tropical moist forests, dozens of species of vascular epiphytes may colonise a single tree exhibiting different physiological, morphological and reproductive adaptations to different micro-sites within the canopy (Benzing 1990, Griffiths & Smith 1983, Hietz & Briones 1998, Johansson 1974). Given the diversity of epiphytes, one may also expect to find differences in their life strategies reflecting the heterogeneity of the canopy. In terrestrial plants two life strategies are commonly distinguished (Crawley 1997). Pioneers are able to colonise an available space quickly and mature fast, but are weak competitors and have short life cycles. Late successional or climax species are slow to colonise and grow, but strong competitors and may live and produce seeds for a long time. In the canopy new branches to be colonised by epiphytes are continuously produced. Since new shoots are mostly produced in the exposed parts of the crown, epiphytes established on these will experience the advantage of abundant light, but will experience more frequent drought stress and high mortality when their supporting branch

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breaks (Hietz 1997). As branches thicken, substrate accumulates, providing more abundant and continuous water and nutrient supply for epiphytes. At the same time, branches are overtopped by others resulting in reduced light and evaporative demand. Pioneers among the epiphytes are the so-called twig epiphytes, mostly orchids of various genera within the Oncidiinae, which show a very strong preference for small twigs and may reproduce within 1 or 2 y (Chase 1987, Warford 1992). A few species of bromeliads and orchids have even been classified as weeds as they can colonise trees at rates that may damage their hosts and become a nuisance to commercial tree growers (Claver et al. 1983, Cook 1926, cited in Curtis 1952, Montaña et al. 1997). Richardson et al. (2000) found that under optimal conditions in a humid tropical dwarf forest, bromeliads grow rather vigorously. Most of the leaves of nine individuals were replaced within 1 y, and bromeliads were estimated to contribute 12.8 % of total forest productivity. Unfortunately neither this nor any other studies explore possible relationships between canopy zones, life histories and growth. Orchids and bromeliads are valued ornamental plants. Collection, often illegal, is seriously endangering some species (Hágsater & Soto Arenas 1998) and areas in Mexico and Guatemala have been practically cleared of saleable Tillandsia species (Schippmann & Zizka 1994). On a sustainable base these activities would not be objectionable and could be an alternative source of income for rural communities and perhaps a valuable non-timber forest product. Without knowing rates of reproduction and growth in the field, however, levels of sustainable harvest cannot be assessed. This paper compares growth rates of different species of epiphytes under natural conditions. Other aspects of population dynamics of these and other epiphytes after 2 y of observations have been published in a previous paper (Hietz 1997). Here we present results of a 5-y field study in a Mexican humid montane forest and discuss differences in

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life histories in the context of the different microclimate and disturbance regimes in the canopy. MATERIAL AND METHODS Study site Field work was carried out in a reserve adjacent to and managed by the Instituto de Ecología in Xalapa, Veracruz, Mexico. According to the Holdridge (1967) life-zone system, the vegetation is intermediate between premontane moist forest and lower montane moist forest and is classified as 'bosque mesófilo de montaña' (mesophylous montane forest, Rzedowski 1986) in Mexico. The average temperature at this altitude (1300 m) is about 19° C, and annual precipitation in Xalapa is 1500 mm, 79% of which falls in the wet season between May and October. The forest structure is described in Williams-Linera (1997) and its epiphyte community and that of a nearby forest in Hietz & Hietz-Seifert (1995a, b). Species Tillandsia juncea and T. butzii exhibit the so-called atmospheric habit by producing only narrow leaves incapable of storing water externally. Tillandsia deppeana and T. multicaulis produce foliar impoundments (phytotelmata) as adults, but have narrow leaves until about 6-10 cm, after which broader leaves appear (Adams & Martin 1986). Tillandsia punctulata has mostly narrow leaves but with broader bases that are able to store small quantities of water in the axils. Catopsis sessiliflora and C. nutans have narrow tanks and produce relatively broad leaves forming a small tank even as juveniles. Ramets of all bromeliads are determinate, flowering once before dying. Tillandsia deppeana is mostly monocarpic, ramets are rarely produced and the plant usually dies after fruiting. All other species are sympodial and polycarpic and produce

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vegetative shoots prior to the death of the first rosette, generally well before the first inflorescence appears. Tillandsia juncea and T.butzii exhibit carbon isotope discriminations typical for CAM plants, the other species perform C3-photosynthesis (Hietz et al. 1999, Martin 1994). Table 1 summarises information about the habit, photosynthetic pathway, reproduction and the distribution within the canopy of the species studied.

Data collection and analysis Between July and September of the years 1992 to 1997, except for 1995, 199 branch sections, about 0.5 to 1.5 m long, were selected on six trees of Quercus germana Schl. & Cham. and one of Quercus xalapensis Humb. & Bonpl. Branches and epiphytes on them were photographed using a Nikon F301 reflex camera with a 50-mm or a 100mm lens. The photographs were scanned with a slide scanner with a resolution of 1350 pixels per inch and analysed with SigmaScan (Jandel Scientific, San Rafael, California, USA) image-processing software. Survival rates were evaluated by comparing the epiphytes on successive photographs of the same branch sections (Fig. 1; Hietz 1997). In most cases plants were classified as 'died' when they had disappeared from the branch or fallen to the ground with the branch, and comparatively few individuals were seen to be dead and still in place. Although fallen epiphytes may not die immediately, their survival on the forest floor is very low (Matelson et al. 1993) and the chance of ever producing successful progeny is virtually nil. The size of bromeliads was measured as the distance from the rosette base to the most distant leaf tip seen, using a disc placed close to the branch as a scale. As the leaves are usually somewhat curved, this measure is generally less than the true length of the longest leaf. To correct for this error for the calculation of

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plant biomass, we correlated measures of 114 plants on photographs with direct measures in the field (sizephotograph = 0.868 x sizetrue, r2 = 0.95). Rosettes photographed from above were excluded, as this perspective considerably shortens the measured length. Leaves were often not parallel to the film and the disc serving as a scale was not exactly at the same distance as the plants. These constraints inevitably introduce some error in the measurements, but there is no reason to expect a systematic bias and for the purpose of this study the rates of change are more important than the absolute values. The height above ground of the photographed branches was measured with a tape, and the branch diameter was measured on the photographs. Growth rates were calculated from a regression between the plant length in year n (ln) and length in year n+1 (ln+1). Because no data were available for 1995 and in other cases plants could not be measured on some photographs, (ln + ln+2)/2 was used for some missing measurements of ln+1. Most small plants could not be determined to the species level, but many of these could be identified when they had grown for several years. Of the 15 species observed, growth curves were calculated only for species with at least 200 year-to-year measurements, and average growth rates are additionally reported for T. butzii. Catopsis nutans and C. sessiliflora, the only members of this genus in the forest studied, could only be distinguished by their inflorescences. Fertile plants of these two species did not differ in diameter (2-tailed t-test, P = 0.80) and the height (P = 0.48) of the branch they were growing on and they were therefore always treated as one group. The growth model was selected from functions offered by the program TableCurve (Jandel Scientific 1991). Criteria for selection were the DOF-adjusted r2, distribution of residuals, simplicity, suitability for all species and whether the form of the curve agreed with a moving average. The function used was ln+1 = a + b x ln + c x ln2 x ln(ln) where ln is the length in year n, ln+1 the length in the following year, and a, b and c are constants obtained

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by curve-fitting. For the most abundant species (T. juncea and T. punctulata) the function was fitted to three randomly selected subsets of equal size, to test the validity of the growth predictions and the dependence on sample size. Using the predicted annual size increments, growth curves were calculated starting with a size of 5 mm. This is a size plants can certainly reach within a year after germination, as individuals of this size were found where definitively no plants had been a year before. From the growth curve and the average size of fertile individuals we calculated the time needed to reach maturity. From the proportion of individuals still present and alive at the time the next photographs were taken, survival rates after exactly 1 y were calculated (see Hietz 1997 for details). The growth curves and the size-dependent survival were used to estimate the probability that a seedling will reach reproductive size. Since small plants could often only be identified to genus we could not distinguish species-specific mortality rates for the smaller size classes and size-dependent mortality was only calculated for the two genera. Mortality in the first year is probably much greater than reported here for the smallest size class, as many seedlings will germinate and disappear without being noted between successive observations. Growth rates were compared between species using only identified individuals of intermediate size classes, which generally showed the highest growth. To calculate biomass from plant size, individual shoots representing the range of sizes of the five species of Tillandsia and of Catopsis were collected from the field, measured, dried and weighed. The size : biomass regression and the relation between the size measured on the photographs and the true size (see above) were used to calculate dry matter (DM) of the leading shoots of photographed plants. Relative growth rate (RGR, mg g-1 d-1) was then calculated as 1000 x [ln(DMyear n+1) - ln(DMyear n)] / ∆t, where ∆t =

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365 to convert to daily growth, which is the more common than per year. This RGR, however, only considers biomass in the leading shoot and does not account for allocation to offshoots. RESULTS The fitted function generally agreed well with the average growth rate over all size classes (Fig. 2). For T. punctulata and T. juncea, where growth curves were calculated for three randomly selected subsets of the data, growth predictions (see below) differed by no more than 1 y. For T. butzii the number of observations was too low to calculate growth curves. Predicted and measured growth of all species of Tillandsia was slow at the beginning (1 - 1.5 cm y-1) and reached about 3 cm y-1 in medium-sized plants of most species (Table 2). Tillandsia deppeana surpassed all of the others with annual increments of > 6 cm. In contrast to Tillandsia, small plants of Catopsis soon grew at 2 cm y-1 and maintained higher rates than Tillandsia until about 8 cm long (Fig. 3). The relationships between maximum leaf length and shoot biomass were described by power functions (Table 3). Relative growth rates generally declined as plants grew (Fig. 4). They were highest in T. deppeana and lowest in T. juncea. This biomass increment, however, only accounts for the largest, and generally oldest, rosette and the investment in offshoots differed strongly. While T. deppeana only occasionally produced small offshoots after reaching reproductive size, most individuals of T. juncea produced several shoots, almost equaling the leading shoot in size, at a very young age. In the other species the leading shoot dominated and gave rise to a varying number of offshoots as plants grew (Fig. 5). RGR declined with size as plants grew, independent of resource allocation to offshoots.

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For intermediate-sized plants with high growth rates, there was a very weak (r2 = 0.0195) but highly significant (Spearman rank correlation, P < 0.001) negative correlation between the distance from the tree top and growth. This correlation was also significant when species, plant size and branch size were accounted for as controlling variables in a partial correlation (P < 0.001). When individual species were tested, the correlation was significant for Catopsis (P < 0.05, Spearman rank correlation), T. juncea (P < 0.01) and T. punctulata (P < 0.05), but not for the others, possibly because of low sample numbers. Branch size had no significant effect on growth rates. Catopsis and T. deppeana reached reproductive size after 9 and 10 y, respectively (Table 4). Catopsis sessiliflora and C. nutans are small plants flowering at about 16 cm, as measured on the photographs, but T. deppeana is by far the largest species studied in terms of biomass. Tillandsia multicaulis and T. punctulata were estimated to reach fertility after 13 y, and T. juncea after 18 y. While the other species kept growing in the year prior to the production of the first inflorescence, growth of T. deppeana practically ceased, and the time to flowering is thus more correctly estimated as 11 y rather than the 10 y required to reach reproductive size. Growth rates predicted from observations of all individuals of a species are averages and faster- and slower-growing individuals will occur. None of the juveniles < 2 cm observed in 1992 had reached fertility after 5 y. The fastest maturation was observed in two individuals of Catopsis that measured little over 2 cm (estimated to be about 2 y at this size) and one individual of T. deppeana with about 5 cm (or 4 y) in 1992 that had become fertile in 1997. This confirms the generally slow maturation predicted for all of the plants studied and the relatively high growth rates of Catopsis and T. deppeana. Survival rates of fertile plants were 0.9-0.96 for polycarpic Tillandsia spp. and 0.74 for Catopsis. Monocarpic T. deppeana normally dies after fruiting, and only in a few

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cases did a small offshoot apparently survive the death of the mother plant. Survival rates in Tillandsia spp. increased with plant size from about 0.6 for plants < 1 cm to 0.83 for size classes >20 cm, confirming earlier results after 2 y of observations (Hietz 1997). In Catopsis, there was no distinct effect of size on mortality. To calculate the probability that a leading shoot reaches fertility, we multiplied survival rates for all growth years from 5 mm to reproductive size. For Catopsis the average survival of 0.68 was taken for all size classes, for Tillandsia survival increased linearly from 0.61 for plants 20 cm and remained constant thereafter. After germination and establishment, the probability of reaching fertility was around 5 % for all species, except for T. juncea (2.8 %). DISCUSSION Growth curves calculated from annual size increments after 5 y reasonably predicted the growth cycle of the bromeliads (Fig. 2). In the humid montane forest studied here 9 to 18 y passed between germination and flowering. This agrees well with the few previous results from epiphytes. Benzing (1981, 1990) found that none of the seedlings of T. pauciflora had flowered after 8 y and estimated that this species requires at least 8-10 y to flower. From an analysis of annual growth, similar to the one presented here, Zotz (1998) estimated that Dimerandra emarginata requires at least 6-10 y to reach the minimum size for flowering. Recent studies have shown that photosynthesis (per leaf area and per unit biomass) in bromeliads and other epiphytes increases with plant size (Zotz 2000). This appears to disagree with the decreasing RGR reported here, also in T. deppeana, which allocates almost no biomass to offshoots. However, maximum photosynthesis is not easily translated to growth rates. As plants grow and become more compact, an increasing

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proportion of their biomass is shaded by other leaves or senescent, and therefore contributes little or nothing to photosynthesis and growth. The higher growth rate of juvenile Catopsis appears to be caused by higher RGR (Fig. 4), the low biomass at a given length (Table 3) and the fact that they do not produce offshoots as precociously as the other polycarpic species (Fig. 5). Generally, differences between species in RGR of the leading shoot can be explained by the number of offshoots produced, and whether these were produced early or later from the parent ramet. For instance, T. juncea, which had the lowest RGR and the longest juvenile stage, had allocated proportionally the most biomass to its offshoots. Growth and RGR of T. deppeana by far exceeded those of the other bromeliads. The other, polycarpic, species divert resources to several offshoots during growth and prior to the production of the first inflorescence. Tillandsia deppeana is not strictly monocarpic and may produce small offshoots, but only when the leading shoot has reached full size and the proportion of biomass allocated to its daughter ramets is minimal. Thus, despite its large size, T. deppeana can flower in just 11 y producing a single branched inflorescence, about 1 m high. Tillandsia deppeana was the species occurring on the most exposed sites and, after Catopsis, on the smallest branches (Table 1). The danger of an epiphyte falling with its supporting branch is strongly dependent on branch size (Hietz 1997, Fig. 6) and especially large plants in exposed positions can also be dislodged by strong winds. Investing all resources in rapid growth leading to one large inflorescence prior to death is a distinct advantage in an environment where the high disturbance imposes high mortality rates (Fig. 6). Similarly, Harper (1977) notes that three terrestrial long-lived biennials (Digitalis purpurea, Dipsacus fullonum and Daucus carota) are also commonly found in locations that experience disturbance, but not annually, which would eliminate the population. When disturbance becomes higher, as on small twigs < 2 cm diameter,

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epiphytes can survive and reproduce only with a very short life cycle, which twig epiphytes achieve by small size and reduced allocation to vegetative parts (Chase 1987). In general, the time required to achieve maturity was shorter for species that tend to grow on thinner or more exposed branches (Fig. 6). This was not an effect of the slightly higher individual growth rates observed closer to the tree top, where branch diameter is smaller: with the exception of T. deppeana, the average growth rate of a species tended to be lower for those growing closer to the tree top (Tables 1 and 2). The fact that the fastest growing bromeliads were found on smaller branches places them between true twig epiphytes, which grow on twigs usually < 2 cm in diameter and reproduce in a few years, and the other bromeliads studied, which grow on longer-lived substrates and take longer to flower. While these epiphytes thus appear to have evolved life cycles reflecting the disturbance regime of their preferred canopy position, it is not clear what causes their distribution in the first place. All of the bromeliads studied produce small, plumed seeds and it appears unlikely that those of Catopsis and T. deppeana preferentially land on smaller branches. Germination rates could differ, depending on substrate humidity and the light climate. Or survival rates could be higher if these species are better adapted to the drier and sunnier conditions on exposed branches or because they hold on firmer to exposed branches. The probabilities that seedlings reached reproductive size were estimated to be between 2.8 and 5 %. However, the mortality of plants representing the smallest size class is certainly underestimated as many seeds will germinate and die before being recorded. Benzing (1978) recorded survival rates of 15 - 80% of 3-mo-old seedlings of Tillandsia paucifolia placed on different hosts and substantially higher survival rates in subsequent years. Given that the average of the smallest size classes was certainly more than 3 mo old, the measured survival rates of 0.6 for Tillandsia spp. and 0.7 for Catopsis spp. < 2

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cm agree well with the report from Benzing. In T. paucifolia the survival of seeds affixed to the substrate was much lower (0.25 to 3.35 %, Benzing 1990). Castro-Hernández et al. (1999), working with Tillandsia guatemalensis in the Chiapas Highlands, with a climate more similar to Xalapa than Florida's, report germination rates of 93-100% for seeds placed on horizontal patches of pine and oak bark. Survival of those seedlings after 7 mo (19.4%) was lower than that of seedlings established naturally after 1 y (34.5%), although the latter had to survive the dry season with much higher seedling mortality. This highlights the potential problems associated with any manipulation of seeds or seedlings in the field. To study population dynamics under natural conditions, field observations cannot easily be replaced by experiments. Whatever natural rates of seedling survival, the chance of a seed landing on a branch and finding a safe site is probably much lower and may be the bottleneck in the life cycle of an epiphyte. For a full account of the population dynamics and population models, rates of reproduction and germination are also needed, but are not accessible by the photographic method used and will be addressed in future studies. ACKNOWLEDGEMENTS Thanks are due to Ursula Hietz-Seifert and Silke Benecke for their help in the field. Gerhard Zotz and three anonymous reviewers made helpful comments to an earlier draft. The hospitality of the Instituto de Ecología in Xalapa is greatfully acknowledged. This research was funded by the Austrian Science Foundation (P-12241-BIO, P14775). LITERATURE CITED ADAMS, W. W., & MARTIN, C. E. 1986. Morphological changes accompanying the transition from juvenile (atmospheric) to adult (tank) forms in the Mexican epiphyte Tillandsia deppeana (Bromeliaceae). American Journal of Botany 73:1207-1214.

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BENZING, D. H. 1978. Germination and early establishment of Tillandsia circinnata Schlecht. (Bromeliaceae) on some of its hosts and other supports in southern Florida. Selbyana 5:95-106. BENZING, D. H. 1981. The population dynamics of Tillandsia circinnata (Bromeliaceae): cypress crown colonies in southern Florida. Selbyana 5:256-263. BENZING, D. H. 1990. Vascular epiphytes. Cambridge University Press, Cambridge. 354 pp. CASTRO-HERNÁNDEZ J. C., WOLF, J. H. D., GARCÍA-FRANCO, J. G., & GONZÁLEZ-ESPINOSA, M. 1999. The influence of humidity, nutrients and light during various stages in the development of the epiphytic bromeliad Tillandsia guatemalensis L.B. Smith. Revista de Biología Tropical 47:763-773. CHASE, M. W. 1987. Obligate twig epiphytism in the Oncidiinae and other neotropical orchids. Selbyana 10:24-30. CLAVER, F. K., ALANIZ, J. R., & CALDÍZ, D. O. 1983. Tillandsia spp.: epiphytic weeds of trees and bushes. Forest Ecology and Management 6:367-372. COOK, M. T. 1926. Epiphytic orchids as a serious pest on citrus trees. Journal of the Deptartment of Agriculture, Puerto Rico 10:5-9. CRAWLEY, M. J. 1997. Life history and environment. Pp. 73-131 in Crawley, M. J. (ed.). Plant ecology. Second edition, Blackwell Science, Oxford. CURTIS, J. T. 1952. Outline for ecological life history studies of vascular epiphytic plants. Ecology 33:550-558. GRIFFITHS, H. & SMITH, J. A. C. 1983. Photosynthetic pathways in the Bromeliaceae of Trinidad: relations between life-forms, habitat preference and the occurrence of CAM. Oecologia 60:176-184.

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HÁGSATER, E. & SOTO ARENAS, M. A. 1998. Orchid conservation in Mexico. Selbyana 19:15-19. HARPER, J.L. 1977. Population biology of plants. Academic Press, London. 782 pp. HIETZ, P. 1997. Population dynamics of epiphytes in a Mexican humid montane forest. Journal of Ecology 85:767-775. HIETZ, P. & BRIONES, O. 1998. Correlation between water relations and within-canopy distribution of epiphytic ferns in a Mexican cloud forest. Oecologia 114:305-316. HIETZ, P. & HIETZ-SEIFERT, U. 1995a. Composition and ecology of vascular epiphyte communities along an altitudinal gradient in central Veracruz, Mexico. Journal of Vegetation Science 6:487-498. HIETZ, P. & HIETZ-SEIFERT, U. 1995b. Intra- and interspecific relations within an epiphyte community in a Mexican humid montane forest. Selbyana 16:135-140. HIETZ, P., WANEK, W. & POPP M. 1999. Stable isotopic composition of carbon and nitrogen and nitrogen content in vascular epiphytes along an altitudinal transect. Plant, Cell and Environment 22:1435-1443. HOLDRIDGE, L.R. 1967. Life zone ecology. Tropical Science Center, San José. 206 pp. JANDEL SCIENTIFIC 1991. TableCurve. User’s Manual. Version 3.0. Corte Madera. JOHANSSON, D. 1974. Ecology of vascular epiphytes in West African rain forest. Acta Phytogeographica Suecica 59:1-129. LARSON, R. J. 1992. Population dynamics of Encyclia tampensis in Florida. Selbyana 13:50-56. MARTIN, C. E. 1994. Physiological ecology of the Bromeliaceae. Botanical Review 60:1-82. MATELSON, T. J., NADKARNI, N. M., & LONGINO, J. T. 1993. Longevity of fallen epiphytes in a neotropical montane forest. Ecology 74:265-269.

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MONTAÑA, C., DIRZO, R., & FLORES, A. 1997. Structural parasitism of an epiphytic bromeliad upon Cercidium praecox in an intertropical semiarid ecosystem. Biotropica 29:517-521. RICHARDSON, B. A., RICHARDSON, M. J., SCATENA, F. N., & MCDOWELL, W. H. 2000. Effects of nutrient availability and other elevational changes on bromeliad populations and their invertebrate communities in a humid tropical forest in Puerto Rico. Journal of Tropical Ecology 16:167-188. RZEDOWSKI, J. 1986. Vegetación de México. Third edition. Editorial Limusa, Mexico, DF. 432 pp. SCHIPPMANN, U. & ZIZKA, G. 1994. "Graue Tillandsien" - ein Fall für den Artenschutz. Palmengarten (Frankfurt a.M.) 58:129-137. STUNTZ, S. & ZOTZ, G. 2000. Photosynthesis in vascular epiphytes. Flora in press. WARFORD, N. 1992. Erycina echinata. American Orchid Society Bulletin 61:568-573. WILLIAMS-LINERA, G. 1997. Phenology of deciduous and broadleaved-evergreen tree species in a Mexican tropical lower montane forest. Global Ecology and Biogeography Letters 6:115-127. ZOTZ, G. 1995. How fast does an epiphyte grow? Selbyana 16:150-154. ZOTZ, G. 1998. Demography of the epiphytic orchid, Dimerandra emarginata. Journal of Tropical Ecology 14:725-741. ZOTZ, G. 2000. Size-related intraspecific variability in physiological traits of vascular epiphytes and its importance for plant physiological ecology. Perspectives in Plant Ecology, Evolution and Systematics 3:19-28.

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Tables Table 1. Habit, photosynthetic pathway and distribution within the canopy of the bromeliads studied in a humid Mexican montane forest. Catopsis spp. comprises C. sessiliflora and C. nutans, which showed identical habit and distribution and could only be distinguished as reproducing specimens. Branch size and distance from tree top are averages for all identified plants of a species. Values accompanied by the same letter are not significantly different (LSD-test, P > 0.05). The effect of branch size and distance from the tree top on species distribution was highly significant (ANOVA, P < 0.0001).

Species

Habit adult

Juvenile Photosynthetic Average Average leaves pathway branch size distance from (cm) tree top (m)

Catopsis spp.

tank

broad

C3

5.5a

5.5bc

T. butzii Mez

atmospheric

narrow

CAM

10.0d

5.8bcd

T. deppeana

tank

narrow

C3

7.4b

4.1a

atmospheric

narrow

CAM

8.9cd

5.8ce

tank

narrow

C3

8.3bc

6.4e

t/a intermediate

narrow

C3

8.9cd

5.4b

Steud. T. juncea Ruíz & Pavón T. multicaulis Steud. T. punctulata Schl. & Cham.


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Table 2. Measured and predicted size increment (maximum leaf length as measured on photographs) of bromeliads in a Mexican humid montane forest. Only intermediate size classes (as indicated) with high growth rates were taken as very small plants and plants approaching full size had lower growth rates. Predicted growth rates are maxima from the function fitted to the annual size increments.

Species

Size class

n

(cm) Catopsis spp.

Growth

Predicted growth

-1

(cm y-1)

(cm y ± SE)

5-12

65

2.3 ± 0.28

2.2

T. butzii

10-25

21

2.8 ± 1.14

T. deppeana

10-28

143

6.3 ± 0.40

6.7

T. juncea

10-35

361

3.3 ± 0.28

3.2

T. multicaulis

10-20

105

3.1 ± 0.35

3.3

T. punctulata

10-20

251

2.8 ± 0.21

3.2


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Table 3. Coefficients of the regression equations of the form DM = a x Llmaxb , where DM = dry mass (g) and Llmax = maximum leaf length (cm). Since T. multicaulis and T. deppeana could not be distinguished up to about 10 cm, such individuals were assumed not to differ in their size : biomass relationship and were attributed to either species in proportion to the number of identified individuals.

b

r2

0.0045

1.97

0.94

46

0.00093

2.09

0.95

T. deppeana

52

0.00059

3.01

0.96

T. juncea

90

0.0014

2.23

0.97

T. multicaulis

126

0.0010

2.64

0.95

T. punctulata

75

0.0024

2.34

0.95

Species

n

Catopsis spp.

43

T. butzii

a


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Table 4. Average length of fertile bromeliads measured as the distance from the rosette base to the most distant leaf tip on the photographs, and the estimated time to reach fertility starting with a size of 0.5 cm after one year. N is the number of size increments used for fitting the growth curve to the function ln+1 = a + b x ln + c x ln2 x ln(ln) where ln is the size in year n and ln+1 that in the subsequent year.

Species

Size of fertiles (cm)

N

Time to fertility

Catopsis spp.

15.8

228

9

T. deppeana

37.8

237

11

T. juncea

42.2

602

18

T. multicaulis

26.8

338

13

T. punctulata

28.5

897

13

(y)


22

Figure captions Fig. 1. Photographs from a sampled branch taken in 1992, 1994 and 1996. The large bromeliad is Tillandsia deppeana. Most of the small individuals seen in 1992 died. Not all individuals are numbered here. Fig. 2. Size change of Tillandsia juncea of individual plants (open circles), averages in 1-cm size classes (solid circles) and fitted growth function ln+1 = 23.7 + 1.10 x ln + 5.22 x 10-5 x ln2 x ln(ln) . Fig. 3. Annual size increments of Catopsis spp. (C. sessiliflora and C. nutans), tank-forming Tillandsia, and atmospheric or intermediate Tillandsia species. Irrespective of the adult habit, all species of Tillandsia studied have atmospheric juveniles until a size of about 8 cm. Whiskers are 1 SE. Fig. 4. Relative growth rates of epiphytic Catopsis and Tillandsia species calculated from measured size increments in six size classes and a regression between shoot biomass and maximum leaf length of the leading shoot. The biomass of offshoots was not accounted for. Note the different y-axis for Catopsis and T. deppeana. Whiskers are 1 SE. Fig. 5. Relationship between maximum leaf length and the number of shoots for epiphytic bromeliads. + in T. deppeana are non-identified broad-leaved individuals that may be either T. deppeana or T. multicaulis. Fig. 6. Probability of a branch breaking (bars), and correlation between preferred branch diameter and the time needed to reach fertility of five epiphytic bromeliads (dots).

Fig. 1. Photographs from a sampled branch taken in 1992, 1994 and 1996. The large bromeliad is Tillandsia deppeana. Most of the small individuals seen in 1992 died. Not all individuals are numbered here.


23

Max. leaf length year n+1 (cm)

60 50 40 30 20 10 0 0

10

20

30

40

50

Max. leaf length year n (cm)

Hietz et al. Fig. 2

60


-1

Size increment (cm y )

6 atmospheric Tillandsia tank Tillandsia Catopsis

5 4 3 2 1 0 0

2

4

6

8 10 12 14 16 18 20 22 24 26

Size (maximum leaf length, cm)

Hietz et al. Fig. 3

24


25

4 3

Catopsis

2 0

-1

-1

RGR (mg g d )

1

2

T.juncea

T.deppeana

1 0 2

T.punctulata

T.multicaulis

5 4 3 2 1 0 2

1

1

0

0 0 20 40 60 80 100

0 20 40 60 80 100

Plant size as % of average fertile size

Hietz et al. Fig. 4


Catopsis

26

T.deppeana 6 5 4 3 2 1

4 3 2 1

Number of shoots

T.multicaulis

T.punctulata 12 10 8 6 4 2

10 8 6 4 2

T.butzii

T.juncea

14 12 10 8 6 4 2

15 10 5

0

10 20 30 40 50

0 10 20 30 40 50 60 70 80

Maximum leaf length (cm)

Hietz et al. Fig. 5

27

Probability of branchfall

0.35

20 18 16 14 12 10 8 6 4 2 0

T. juncea

0.30 0.25 T. multicaulis

0.20

T. punctulata T. deppeana

Catopsis

0.15 0.10 0.05 0.00 0

Hietz et al. Fig. 6

2

4

6 8 10 12 Branch diameter (cm)

14

Years to fertility
