Effect of Elevation on the Composition of Canopy Epiphytes Lew 1 Effect of elevation on the composition and eco physiological strategies of canopy epiphytes in a tropical montane cloud forest Christina Lew Department of Environmental Science, Policy, and Management University of California, Berkeley EAP Tropical Biology and Conservation Program, Fall 2016 16 December 2016 ABSTRACT Tropical montane cloud forests have a high diversity and abundance of epiph ytes that have drought resistance adaptations to the water and nutrient limitations in the canopy. Most epiphytes in the canopy ha ve drought adaptations and may have d ifferent distributions along the vertical gradient of a single tree in addition to varying at a landscape scale such as with elevation. Vascular epiph yte composition and eco physiological strategies were studied along an elevational gradient of 1400 1830m in a cloud forest in Monteverde to see if there is a variation in diversity, abundance, and drought adaptation characteristics. I measured m orphospecies diversity, abundance, foliar water uptake capacity, and leaf toughness for epiphytes on fallen branches The prevalence of other traits such as succulence, trichomes, and pseudo bulbs in orchids were also compared across elevations. I also measured the canopy cover, branch diameter, and humus mat thickness of eac h branch measured to look at preferred local s ubstrate characteristics No significant trends were found between elevation and epiphyte morphospecies diversity, abundance, foliar water uptake capacity, or leaf toughness even among individual families. There were slight positive trends between morphosp ecies diversity with branch diameter and humus mat thickness which may suggest that local substrate preferences are more influential in determining the composition of epiphytes rather than large scale characteristics like elevation. Efecto de la elevaciÂ—n sobre la composiciÂ—n y las estrategias ecofisiolÂ—gicas de las epÂ’fitas de dosel en un bosque montano tropical RESUMEN Los bosques nubosos tropicales presentan una alta diversidad y abundancia de epÂ’fitas, las cuales presentan adaptaciones para resistir la limitaciÂ—n de agua y nutrientes en el dosel del bosque. La mayorÂ’a de epÂ’fitas en el dosel podrÂ’an presentar diferentes distribuciones a lo largo del gradiente vertical de un Â‡rbol, asÂ’ como diferencias a una mayor escala a l o largo de un gradiente altitudinal. EstudiÂŽ la diversidad de morfoespecies, abundancia de epÂ’fitas vasculares y sus adaptaciones ecofisiolÂ—gicas a lo largo de un gradiente altitudinal entre 1400 1830 m s.n.m. en el bosque nuboso de Monteverde. AdemÂ‡s est udiÂŽ la variaciÂ—n de estrategias ecofisiolÂ—gicas de resistencia a desecaciÂ—n a lo largo de este gradiente. La estrategias estudiadas fueron capacidad foliar de absorciÂ—n de agua y dureza de hojas, ademÂ‡s de la prevalencia de suculencia, tricomas y psedobul bos en las plantas. Las muestras provinieron de ramas caÂ’das. AdemÂ‡s medÂ’
Effect of Elevation on the Composition of Canopy Epiphytes Lew 2 la cobertura de dosel, diÂ‡metro y grosor de la cobertura de musgo de cada rama para determinar el efecto del sustrato sobre las variables. No encontrÂŽ correlaciÂ—n de ninguna variable con la altitud dentro de cada familia encontrada. EncontrÂŽ una tendencia positiva en la correlaciÂ—n entre diversidad de morfoespecies con diÂ‡metro de rama y grosor de la capa de musgo. Esto sugiere que variaciones a nivel local dentro de cada Â‡rbol hosped ero tienen mayor influencia sobre la composiciÂ—n de epÂ’fitas que variables de mayor escala como la elevaciÂ—n. Canopy plants are important for the hydrological cycle of tropical forests due to their high water storage capacity and additional surface area, which increases cloud and rainwater interception and provides ad dit ional water to the ecosystem. The water can be stored and be input into the environment at a later time, with water slowly dripping down into the communities on the ground (Kohler et al. 2007, Holder 2003). Epiphytes comprise 30% of the total foliar biomass and 45% of the nutrient capital in the cloud forest of Monteverde (Nadkarni 1984 ). They also increase the number of dense mats of soil and mos s in the canopies by holding together orga nic matter with their roots, therefore increasing the water holding capacity of the forest in addition to providing shelter for many organisms (Nadkarni et al. 2004). Montane cloud forests are common in the tropics where moist air rises abruptly due to r apid changes in elevation with the water vapor condensing at ground level (Holder 2003). This change in elevation over a short distance results in heterogeneous climates and diverse patches of vegetation in a small area (Holder 2003). Epiphytes exist in mi croclimates along the vertical tree gradie nt and at a larger regional scale. Conditions such as temperature, sun exposure, water input, humidity, and wind can change from the ground to the canopy and along an elevational gradient (Wolf & Flamenco 2003) Th e distribution of epiphytes can also be dependent on local substrate characteristics like the host tree's size and age along with the diameter and structure of its branches (Nadkarni et al. 2004). Most epiphytes have some xeromorphic adaptations to life in the canopy which is especially important due to their slow growth because of the intermittent supply of water and nutrients (Bartels & Chen 2012). Epiphytes increasing in height towards the canopy are usually faced with drier and harsher conditions and ha ve evolved adaptations to deal with the drought like conditions and instability of the canopy (Kromer & Kessler 2006) Because of this, the highes t species richness is usually found to be in the inner and intermediate canopy zones with orchids and ferns being the most diverse of vascular epiphytic species (Kromer & Kessler 2006). Most vascular epiphytes have xeric adaptations like coriaceous leaves, succulence, adventitious roots (roots rising from the stem rather than from primary root system) mycorrhizal associations, low rates of water loss, leaf scales or tri chomes, and water storage structures (Hietz & Briones 1997). Species found in exposed conditions had thicker leave s, more but smaller stomata, stiff cell w alls and high turgor loss point (Martin 1994) Storage of water in succulent tissue or fleshy roots, stems, petioles, and peduncles is also common across epiphyte families (Madison 1977). Epiphytes rely heavily on t he branch humus consisting of mats of moss, lichens, canopy soil, and plant litter which is a major source of mineral nutrients and water. They are also important substrates for the roots of epiphytes to attach to as weather conditions in the canopy are us ually stronger than on the forest floor (Madison 1977). More than 99% of the genera of vascular epiphytes have species with adventitious roots that allows them to attach to
Effect of Elevation on the Composition of Canopy Epiphytes Lew 3 the substrate in many places, in addition to being able to reach more water and nut rients (Madison 1977). Epiphytes across families exhibit much v ariation in functional strategies rela ting to drought avoidance or tolerance (Gotsch et al 2015). Epiphytes are able to absorb water through their leaves when the clou d water condenses on the m. A faster rate of absorption would be more beneficial and this may depend on how thick the cell wall is and how long water is able to stay retained on the leaf Many species have been shown to have the capacity for the foliar uptake of water which also c ontributed significantly to their water balance (Gotsch et al 2015 Martin 1994). Foliar uptake occurs when atmospheric droplets condense on plant shoots and move along a water potential gradient from the outside of leaves and stems into internal tissues which increases water content of the leaves and plant water potential (Limm et al. 2009). Studies have measured direct water absorption into removed leaves by cutting a mature leaf that were young and fully mature and measuring the amount of water it can a bsorb when fully submerged (Limm et al. 2009). Leaf toughness can be an indicator of the cell wall thickness, the number of cells that water has to pass through into the leaves, and the ability of water to withstand the pressure of precipitation. Leaf toug hness is typically measured by the weight a leaf can handle before it breaks (Gotsch et al. 2015). Other common xeromorphic traits in epiphytes include succulence, pseudobulbs in orchids, and trichomes. Succulence is the storage o f water in the leaves, stems, or petioles which is evident in fleshy and often translucent appearance in these areas (Madison 1977). Pseudobulbs are water storage structures found in some species of orchids and they are a drought resistance adaptation such that individuals can survive prolonged periods of drought (Benzing 1995). T richomes are commonly found in bromeliads, which are small hairs on the leaves or stem s that can help collect and retain water which can increase the rate of foliar water uptake (B enzing 1995). In addition to these physiological traits, the substrate characteristics of the host tree can greatly influence the composition of epiphytes. The th ickness of the humus mat consisting of moss and lichens that epiphytes use to penetrate their roots in and to a cquire nutrients and water can determine which species are present and how many individuals can be supported on that branch (Nadkarni et al. 2004). There may be too much competition for nutrients between the vascular and non vascular epiph ytes at thin humus mats and perhaps too large of a water input at thick mats since most epiphytes have drought resistant adaptations. Branch diameter has also been found to influence the abundance of epiphytes as this determines how much space is available for epiphytes to establish (Bartels & Chen 2012). Studying the habitat preferences and water relations of these diverse vascular epiphytes in tropical cloud forests is important for looking at the effects of climate change on these abundant communities, which can significantly affect the forest's hydrological cycle. The questions I will be addressing are: 1) How does species richness and abundance of epiphytes change with elevation and substrate type? 2) Is there a difference in abundance of certain eco p hysical traits to deal with canopy conditions along an elevational gradient? To study this, I compared diversity and abundance of vascular epiphytes across an elevational gradient. I also measured the foliar water uptake capacity and leaf toughness of ever y morphospecies I found to see if there was a variation increasing in elevation. I also looked at the presence of certain eco physiological traits like succulence, pseudobulbs in orchids, and trichomes along the studied range. In addition, I
Effect of Elevation on the Composition of Canopy Epiphytes Lew 4 analyzed subst rate preference by measuring the branch diameter and humus mat thickness that the epiphytes were found on. MATERIALS & METHODS I collected vascular epiphytes from fresh fallen branches but not from fallen trees along the trails in the cloud forest adjac ent to the EstaciÂ—n BiolÂ—gica Monteverde Costa Rica leading to the TV towers from 25 November 2016 30 November 2016. The elevation range is 1400 1850m in this area, which is a narrow enough elevation for all the samples to be in the same life zone, the montane cloud forest Fallen branches were used instead of surveying the canopy because of the abundance available and accessibility. A recent storm provided many freshly fallen branches so it is fairly certain that the plants on each branch were from the canopy rather than plants that established after falling Each branch was measured for branch diameter and the th ickness of the humus mat on to p at the thick est section of the branch. Altitude was measured using an altimeter at each branch. Only true epiphytes (plants that never have their roots in the ground at any point of their life) were considered, excluding hemi epiphytes and non vascular m oss and lichens. I measured and collected from any branch that I came across on the trail. Branc hes of all sizes were collected. Each branch was then sorted for the number of individuals and morphospecies. Each individual was given a morphospecies label on ly based on morphological differences on a family level rather than being identified to genus or species level. All ferns were grouped into Pteridophyta. The largest mature leaf from the largest individual of every species on each branch was measured for foliar water uptake capacity and leaf toughness. Foliar water uptake capacity was measured by removing a leaf from the plant, cleaning the leaf of organic matter and water, and measuring the initial weight. The entire leaf was then submerged in a beaker o f water for 3 hours (submerged time based on Limm et al. 2009 study), removed after that time, towel dried of excess water, and measured again for the final weight. This value was subtracted from the initial weight value to measure the amount of water the leaf was able to absorb in three hours. Leaf toughness was then measured using a penetrometer on a single leaf. The leaf was placed in between two metal blocks with a sharp pin connected to a platform resting on top. The sharp pin was placed on the leaf, avoiding the lateral vein which would be tougher than the foliar parts. A 600mL beaker was placed on top of the platform and slowly filled with water until the pin broke through the leaf. The volume of water in mL needed for the pin to break through the l eaf was used as the indicator for leaf toughness. If the leaf broke through immediately upon placement of the empty beaker, the leaf toughness was recorded as 0 mL Leaves that were smaller than the size of the pin were not measured for leaf toughness. Pla nts were also noted for succulence (in stem, petioles, or leaves), presence of trichomes or leaf scales, and presence of pseudobulbs in orchid morphospecies. RESULTS A total of 61 branches were collected, with 11 families, 666 individual plants and 309 of those were used for functional trait measurements (Table 1) The total number of morphospecies found among all families were 116. The most diverse species were Orchidaceae with 53 morphospecies and Pteridophyta with 30 morphospecies (Figure 1). They als o spanned the most
Effect of Elevation on the Composition of Canopy Epiphytes Lew 5 elevations ranging from 1440 1830m and 1440 1830m respectively. These two groups were also the most abundant with 273 individuals found in Orchidaceae and 193 individuals in Pteridophyta. Across all morphospecies, the leaf toughness ranged from 0 800 mL and the foliar water uptake capacity ranged from 0.084 0.264g. The percentage of morphospecies with succulence was 36.3% and with trichomes 14.1% across all families. The percentage of orchid morphospec ies with pseudobulbs was 65.4% Table 1: Sample size (N* ) of individuals measured for functional traits, average foliar water uptake capacity (g), average leaf toughness (mL), total number of morphospecies, % morphospecies with succulence, and % morphospecies with trichomes in each family. All morphospecies were grouped together for the average foliar water uptake capacity and average leaf toughness. The results show no significant trend in elevation in relat ion to the abundance, diversity or water relations of canopy epiphytes (Figures 4 5). There were some slight trends in a few families but were not significant. Some families with a low sample size (less than 6 individuals) were excluded from abundance and diversity comparisons and functional trait measurements. Even among families, the foliar water uptake capacity and leaf toughness were generally constant throug hout all elevations. All morphospecies were found to have the capacity for foliar water uptake. However, some values were negative which means that water volume was lost during the submersion time. The number of individuals with pseudobulbs in Orchidaceae and the number of individuals with trichomes were also relatively constant along th e elevational gradient (Figures 6 7). However, the morphospecies of individuals with trichomes in each family seems to be restricted to certain elevational ranges with Bromeliaceae only occurring in 1450 1550m and Pteridophyta in 1550 1850m. There appears to be a slight positive correlation between th e Family n N n morphospecies Morpho species with Trichomes Morpho species with Succulence Avg Foliar Water Uptake Capacity (g) Avg Leaf Toughness (mL) Araceae 3 2 2 0.029 0.018 250 50 Bromeliaceae 98 42 8 12.50% 0.442 0.020 240 118 Clusiaceae 7 5 4 100% 0.026 0.027 450 141 Ericaceae 6 6 6 16% 6 0.360 0.180 335 187 Gesne riaceae 1 1 1 100% 0.047 0 Melastomataceae 6 4 1 25% 0.751 0.020 180 209 Orchidaceae 273 107 53 41% 0.018 0.037 351 179 Piperaceae 60 35 9 100% 0.002 0.005 246 114 Pteridophyta 193 94 30 20% 3.33% 0.022 0.053 163 162 Urticaceae 2 2 2 0.036 0.035 37.4 53.0
Effect of Elevation on the Composition of Canopy Epiphytes Lew 6 number of morphospecies with the diameter of the host branch and the thickness of the moss mat (Figure 8). Both Pterido phyta and Orchidaceae were the most abundant groups across all elevations, up to 15 individuals at various elevations, (Figure 1) compared to Piperaceae and Bromeliaceae which were under 5 individuals. The same is true for the number of morphospecies, with Orchidaceae and Pteridophyta being the most diverse across all elevations (Figure 2). For foliar water uptake capacity, there again does not appear to be any significant trends with elevation (Figure 3). Orchidaceae and Pteridophyta have more variation in foliar water uptake rates than in Bromeliaceae and Piperaceae and also have individuals with higher capacities. Leaf toughness appears to not be correlated to elevation at all with different values generally at all elevations in each family (Figure 4). The number of individuals with the presence of succulence, trichomes, and pseudobulbs also remained relatively constant throughout the elevational range studied (Figure 5). However, when looking at the morphospecies diversity throughout the elevational gra dient, there seems to be a slight positive correlation with the number of morphospecies with each the humus mat thickness and branch diameter.
Effect of Elevation on the Composition of Canopy Epiphytes Lew 7 Figure 1: Abundance of individual samples in the most abundant families Pteridophyta, Piperaceae, Orchidaceae and Bromeliaceae along the studied elevational gradient. Other families were excluded because of low sample sizes (<6). Figure 2: Number of morphospecies in the most abundant families Pteridophyta, Piperaceae, Orchidaceae, and Bromeliaceae along the studied elevational gradient. Other families were excluded because of low sample sizes (<6).
Effect of Elevation on the Composition of Canopy Epiphytes Lew 8 !" !#!$" !#!%" !#!&" !#!'" !#!(" !#!)" !#!*" !#!+" $'(!" $((!" $)(!" $*(!" ,-./01"20341"563074"80608/39":;<" 0.3/35=4":><" 8?@ABCDECE" >E?CAFGHCFCDECE" 4IBDCDECE" Figure 3: Top four Foliar water uptake capacity (g) of the most abundant families. Left Clusiaceae, Melastomataceae, Ericaceae. Foliar water uptake capacity is in mL of water absorbed by a single leaf in three hours. One leaf from one individual of every species on each branch was measured. J"K"&4L!)M"N"!#!!('" 1O"K"!#!!!%+" !" !#!(" !#$" !#$(" !#%" !#%(" $'(!" $((!" $)(!" $*(!" $+(!" 20341",-./01"563074"80608/39":;<" 0.3/35=4":><" PIGHE?BCDECE"
Effect of Elevation on the Composition of Canopy Epiphytes Lew 9 J"K"L$#%*)'M"N"%(!*#)" 1O"K"!#''%**" J"K"L!#++)(M"N"$+)'#%" 1O"K"!#$%&*&" J"K"L!#*+((M"N"$'$+#%" 1O"K"!#&$!%*" !" $!!" %!!" &!!" '!!" (!!" )!!" *!!" $'(!" $((!" $)(!" $*(!" $+(!" .40,"3-5;QR4SS":>.<" 0.3/35=4":><" 8?@ABCDECE" 4IBDCDECE" >E?CAFGHCFCDECE" Figure 4: Top four Leaf toughness (mL) of the most abundant families. Left Clusiaceae, Melastomataceae, Ericaceae. Leaf toughness is in mL of water needed in a 600 mL glass beaker to penetrate a leaf. One leaf from one individual of every species on each branch was measured.
Effect of Elevation on the Composition of Canopy Epiphytes Lew 10 Figure 4: The number of individuals with succulence in either the leaf, stem, or petiole in families Orchidaceae, Piperaceae, Clusiaceae, Ericaceae. Figure 5: Left The number of individuals among all morphospecies in the families Bromeliaceae, Pteridophyta and unknown identification with trichomes on either the leaves, stem, or petioles. Right The number of individuals that have pseudobulbs in the Orchidaceae family.
Effect of Elevation on the Composition of Canopy Epiphytes Lew 11 J"K"!#!'$&M"N"%#'+%" 1O"K"!#!()+" !" (" $!" $(" %!" %(" !" (!" $!!" P10R8Q"=/0>4341":>><" Figure 6: Left The number of morphospecies across all families at various humus mat thickness (mm). Right The number of morphospecies across all families at various branch diameters (mm). DISCUSSION Although elevation can produce micro climatic differences in the landscape scale causing variations in rainfall, humidity and temperature in a small area epiphyte composition does not appear to be influenced by an elevational range as narrow as 400m. There was little evidence that e levational gradients drive patterns of species richness abun dance, or prevalence of certain eco physiological traits on this spatial scale Previous studies have found that the mid domain effect had the most impact on epiphyte distribution (Kromer & Kessler 2006, Kromer et al. 2005, Sanger & Kirkpatrick 2015, Watki ns et al. 2006, Wolf & Flamenco 2003) The mid domain effect says the ecological or hard boundaries at the top and bottom of gradients force the overlap of species toward the middle of domains which result in the peak of diversity which would explain the f requently found humped distribution of diversity and elevation where richness of epiphytes is highest at mid elevations (Watkins et al. 2006). S tudies of ferns, bromeliads, and orchids ranged from sea level to 2000m in elevation and found the highest diver sity of epiphytes at mid elevations (Wolf & Flamenco 2003). However, this study did not find a humped distribution or any significant trends on the effect of elevation and the diversity and abundance of canopy epiphytes even within families. This may be be cause of the narrow elevation range that was analyzed in this study. It may not be significant enough to impact the composition of epiphytes, which may also be a result of the life zone I studied. The tropical montane cloud forest's input of atmospheric cl oud water may be uniform across this narrow elevation range and provide enough additional water to support a large number and diversity. In addition, ferns are typically found to be generalist species which may explain their presence and abundance in all the elevational ranges studied (Watkins et al. 2006). It appears that traits like foliar water uptake capacity and leaf toughness do not differ in distribution across elevational gradients as various values were present in almost all the ranges studied. T he number of m orphospecies with succulence and trichomes do not make up the J"K"!#$&T(M"N"'#)(*$" 1O"K"!#!$*'&" !" (" $!" $(" %!" %(" !" (" $!" $(" %!" U"-,">-16Q-S648/4S" >03"3Q/87R4SS":>><"
Effect of Elevation on the Composition of Canopy Epiphytes Lew 12 majorit y of canopy epiphyte diversity at 36.3% and 14.1% respectively. The % of morphospecies found with pseudobu lbs in orchids were high (65.4%) but did not increase in prevalence at higher altitudes. Many of these eco physiological traits may be restricted to taxonomy and phylogenetic history, which may be a reason this elevational range did not have an influence o n the composition of epiphytes. Orchidaceae may be high in abundance and diversity because of the many xeromorphic characteristics species in this family possess that can take advantage of the atmospheric water source. Many morphospecies were found to hav e fleshy succulent leaves a nd pseudobulbs that store water, reducing desiccation at times of drought. Basket like structures formed by negatively geotropic roots that accumulate litter and water are present in many orchids (Madison 1977). The orchid aerial roots have spongy velamen cells that can collect atmospheric water and nutrients directly from the atmosphere (Benzing 1995). It was not a surprise to find ferns to be abundant and highly diverse across all elevations since this group is present in many habitats and climates across the world. Almost all bromeliads can collect water and litter in tightly overlapping leaf bases tha t form water storage tanks (Madison 1977). Many species of bromeliads like the genus Tillandsia have leafy shoots with absorptive trichomes that retain and direct water towards these tanks (Benzing 1995). These foliar trichomes also help collect nutrients and throughfall that can be absorbed through the leave s (Cardelus & Mack 2010). However, Local host tree scale characteristics seem to have more impact on the composition of epiphytes. There is a slight positive trend on the number of morphospecies with b ranch diameter. A larger plant diameter would allow for more individuals to inhabit the branch and perhaps more space to reduce competition between species for space and resources. There also appears to be a slightly positive correlation between for the nu mber of morphospecies and the thickness of the humus mat. There were several limitations and sources of error in this study. Using only epiphytes found on fallen branches may have underestimated the diversity and abundance. Not being able to have a compl ete sample of the canopy would underestimate the diversity present in the canopy. Misidentifications of morphospecies could have led to under or over estimations of species diversity. Orchids are the richest family of epiphytes with many that are unable t o be identified based on morphology without the presence of the flower. Comparing abundance, diversity, foliar water uptake capacity, and leaf toughness would also have been useful to compare at the genus level rather than clumping all morphospecies in the ir families which would lose a lot of diversity. The functional trait measurements might also differ in rates of water absorption depending on the thickness and morphology of the leaves so comparing within families may have been more informative. Other sou rces of error in the functional trait measurements may have been due to the accuracy of the scale. Increased precision and would be necessary for continued studies because the weight of water entering the leaves may be miniscule if the leaves themselves ar e very small. I also obtained some negative values in foliar uptake capacity that may have been due to the accuracy of the scale, which I omitted from my results. A negative value would mean that water was being lost from the leaves while fully submerged r ather than being absorbed. This could also have been because some leaves are difficult to completely clean of extra organic matter, which would influence the weighing if there were some present during the initial weighing, and was washed off while being su bmerged in water. However, this study leads to further questions on what regional factors would influence the water relations and composition of canopy epiphytes. Since they make up such a large biomass and greatly contribute to the hydrological and nutrient cycles in the t ropical montane
Effect of Elevation on the Composition of Canopy Epiphytes Lew 13 cloud forest, it is important to know how the diversity and abundance of epiphytes would be affected by climate change. Since these plants have many xeromorphic adaptations and already live in a highly variable climate, it would be interest ing to how epiphyte composition would be affected by the changing temperature and precipitation patterns of the tropical forests. Since e piphytes may be better adapted to deal with weather fluctuations, extreme precipitation, o r increased periods of drough t it is possible that epiphytes may not be as affected as terrestrial plants in tropical forests. Future studies should include canopy surveys to get a more complete analysis of the diversity of canopy plants species and eco physiological strategies that a re present in epiphytes. It would be interesting to see at what point of the elevational range would there start to be differences in the composition of epiphytes, so studies at larger elevational gradients would be necessary. It is also important to conti nue studies on atmospheric water input and epiphytic water physiology to see how much epiphytes actually use this water source ACKNOWLEDGEMENTS Thank you to Andres Camacho for the endless advice and for hiking for hours with me to collect my samples. Thank you to Sofia Arce Flores for th e feedback on my paper and to Eladio Cruz for helping me identify my many plants. Thanks to F ederico Chinchilla and Frank Joyce for being always available to help. Thanks to the Monteverde Institute and the Monteverde B iological Station for allowing me to use their space and resources. WORKS CITED Bartels, S.F. & Chen, H.Y.H. 2012. Mechanisms regulating epiphytic plant diversity. Critical Reviews in Plant Sciences. 31:391 400. Benzing D.H. 1995. The physical mosaic and plant variety in forest canopies. Selbyana, 16(2): 159 168. Cardelus, C.L. & Mack, M.C. 2010. The nutrient status of epiphytes and their host trees along an elevational gradient in Costa Rica. Plant Ecology. 207: 25 37. Gotsch, S.G.; Nadkarni, N.; Darby, A.; Glunk, A.; Dix, M.; Davidson, K.; & Dawson, T.E. 2015. Life in the treetops: ecophysical strategies of canopy epiphytes in a tropical montane cloud forest. Ecological Monographs. 85(3): 393 412. Hietz, P. & Briones, O. 1997. Correlation between water relations and within canopy distribution of epiphytic ferns in a Mexican cloud forest. Oecologia. 114: 305 316. Kromer, T. & Kessler, M. 2006. Vertical stratification of vascular epiphytes in submontane and montane forest of the Bolivian Andes: the importance of the understory. Plant Ecology. 189:261 278. Kromer, T.; Kessler, M.; Gradstein, R.; & Aceby, A. 2005. Diversity patterns of vascular epiphytes along an elevational gradient in the Andes. Journal of Biogeography. 32 (10): 1799 1809.
Effect of Elevation on the Composition of Canopy Epiphytes Lew 14 Limm, E.B.; Simonin, K.A.; Bothman, A.G. & Dawson, T.E. 2009. Foliar water uptake: a common water acquisition strategy for plants in the redwood forest. Oecologia. 161: 449 459. Madison, M. 1977. Vascular epiphytes: their systematic occurr ence and their salient features. Selbyana. 2(1): 1 13. Martin, C. E. 1994. The physiological ecology of the Bromeliaceae. Botanical Review. 60(1): 1 82. Nadkarni, N. M. 1984. Epiphy te biomass and nutrient capital of a neotropical elfin forest. Biotropica 1 6(4):249 256. Nadkarni, N.M.; Schaefer, D.; Matelson, T.J.; & Solano, R. 2004. Biomass and nutrient pools of canopy and terrestrial components in a primary and a secondary montane cloud forest, Costa Rica. Forest Ecology and Management. 198(223 236). Sange r, J.C. & Kirkpatrick, J.B. 2015. Moss and vascular epiphyte distributions over host tree and elevation gradients in Australian subtropical rainforest. Australian Journal of Botany. 63: 696 704. Watkins, J.E.; Cardelus, C.L; Colwell, R.K.; Moran, R.C. 2006 Species richness and distribution of ferns along an elevational gradient in Costa Rica. American Journal of Botany. 93(1): 73 83. Wolf, J. H. D. & Flamenco, A. 2003. Patterns in species richness and distribution of vascular epiphytes in Chiapas, Mexico. Journal of Biogeography. 30:1689 1707.