Thesis, University of Amsterdam, the Netherlands

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Vascular epiphytes in Taiwan and their potential response to climate change

Hsu, R.C.C.

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UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:10 Oct 2021 Vascular epiphytes in Taiwan and their potential response to climate change Rebecca C.-C. Hsu

2013 UNIVERSITEIT VAN AMSTERDAM Cover: The epiphytic fern Polypodium formosanum growing on a blue glass ball (representing the Earth) to express that species' response to climate change is an entangled question.

Back cover: A common scenery of montane cloud forests in the afternoon on Taiwan.

Vascular epiphytes in Taiwan and their potential response to climate change

Hsu, R. C.‐C. 2013. Vascular epiphytes in Taiwan and their potential response to climate change.

PhD thesis, University of Amsterdam, The Netherlands

Cover layout: Rebecca C.‐C. Hsu Cover illustration: Rebecca C.‐C. Hsu ISBN: 978‐94‐91407‐12‐3 Vascular epiphytes in Taiwan and their potential response to climate change

ACADEMISCH PROEFSCHRIFT

ter verkrijging van de graad van doctor aan de Universiteit van Amsterdam op gezag van de Rector Magnificus prof. dr. D.C. van den Boom ten overstaan van een door het college voor promoties ingestelde commissie, in het openbaar te verdedigen in de Agnietenkapel op dinsdag 10 september 2013, te 10.00 uur

door

Rebecca Chia‐Chun Hsu

geboren te HsinChu, Taiwan

Promotiecommissie

Promotores: Prof. dr. G.R. de Snoo Prof. dr. J.H.D. Wolf Copromotores: Dr. J.G.B. Oostermeijer Dr. W.L.M. Tamis

Overige leden: Dr. J.F. Duivenvoorden Prof. dr. H. Hooghiemstra Prof. dr. S.B.J. Menken Dr. N. Raes Prof. dr. P.H. van Tienderen

Faculteit der Natuurwetenschappen, Wiskunde en Informatica CONTENTS

1 General Introduction 6

2 Diversity and phytogeography of vascular epiphytes in a tropical‐subtropical transition island, Taiwan (Flora 204(8), 2009, pp. 612‐627) 16

3 Regional and altitudinal patterns in vascular epiphyte richness on an East Asian island 30

4 Canopy CO2 concentrations and crassulacean acid metabolism in Hoya carnosa in a subtropical rain forest in Taiwan: consideration of CO2 availability and the evolution of CAM in epiphytes (Photosynthetica 44(1), 2006, pp. 130‐135) 48

5 Comparative photosynthetic capacity of abaxial and adaxial leaf sides as related to exposure in an epiphytic fern in a subtropical rainforest in northeastern Taiwan (American Fern Journal 99(3), 2009, pp. 145-154) 60

6 Adaptation of a widespread epiphytic fern to simulated climate‐change conditions 70

7 Simulating climate change impacts on forests and associated vascular epiphytes in a subtropical island of East Asia (Diversity and Distributions 18(4), 2012, pp. 334-347) 86

8 Conclusions 108

REFERENCES 115 APPENDIX 1 139 APPENDIX 2 149 SUMMARY 159 總結 163 SAMENVATTING 169 ACKNOWLEDGEMENTS 175 Chapter 1 General Introduction

The medium (category‐2) typhoon Morakot (2009) brought 2777 mm rainfall in 72 h, causing catastrophic damage. Numerous uprooted trees and associated epiphytes were brought by floods to the coast. CHAPTER 1

General Introduction

The distribution of vascular epiphytes

Epiphytic plants are a characteristic component of the tropical wet forest (Benzing, 1990). In this thesis, epiphytes are defined, following Barkman (1958), as organisms that grow on plants without extracting water or nutrients from hosts’ living tissues. Unlike parasitic plants, epiphytic plants are autotrophic depending only on their hosts for anchorage whilst obtaining essential resources by intercepting dry and wet depositions (e.g. dust, litter, rainfall and fog). It is not rare to find so‐called accidental epiphytes growing on other plants; however, those are mostly unable to reproduce in the canopy (Moffett, 2000).

The focus in this thesis is on vascular epiphytic plants, whereas many other organisms such as bryophytes and lichens can also be found growing as epiphytes in the forest canopy. Based on their life history, vascular epiphytes can be classified into true epiphytes (holo‐epiphytes) and hemi‐epiphytes (Schimper, 1888). The former complete their entire life cycle without contacting the forest floor, whilst individuals of the latter spend part of their life cycle as terrestrial plants. The epiphytic life‐form is a successful adaptation of plants to the forest canopy, comprising ca. 29,000 species, or approximately 10% of all vascular plants, in 83 different families and 876 genera (Gentry and Dodson, 1987a). Epiphytes are unevenly distributed over taxonomic groups and geographic locations. The epiphyte flora is concentrated in monocotyledons, especially orchids, bromeliads and aroids, and in ferns and fern‐allies (Benzing, 1990). With few exceptions, epiphytic vascular plants are mainly found in the tropical region (< 23.5° latitude). In contrast to the Neotropics, paleotropical areas lack several species‐rich epiphytic families (e.g. Bromeliaceae, Cactaceae and Marcgraviaceae) and have received less attention from botanists. Especially from Asia, epiphyte inventories are still rare (Wolf and Flamenco‐S, 2003).

Whereas epiphyte richness generally decreases with latitude, numerous studies have reported a different pattern in richness along the altitudinal gradient on mountains. Apparently epiphytes (and many other organisms) achieve greatest diversity at mid‐elevations although the altitudinal position of the diversity maximum may vary among geographical areas (Wolf and Flamenco‐S, 2003; McCain, 2004; Kromer et al., 2005; Cardelus et al., 2006; Laurance et al., 2011). Some studies (e.g. Cardelus et al., 2006) suggest that the observed hump‐shape in species richness can best be explained by a null distribution (i.e. the mid‐domain effect, MDE). The MDE arises from geographic constraints on species ranges within a bounded domain (e.g.

INTRODUCTION from coasts to mountaintops) whereby the null model predicts that overlapping species’ ranges lead to a peak in species richness at mid‐elevation (Colwell and Lees, 2000). However, it has been argued that the MDE has been overstated in the past and that climatic factors are closely related to species richness patterns (Kessler et al., 2011). Moreover, island and continental systems seem to demonstrate different elevational diversity patterns. For instance, whereas MDE provided a reasonable explanation for bryophyte richness in the continental Andes, MDE underestimated the species richness at mid‐elevation in an Indian Ocean island (Ah‐Peng et al., 2012). The exceptional high species richness at mid‐elevation on this island reflects the presence of a large number of species with a small range size, presumably due to climatic compression. Another explanation for the unbalanced proportion of narrow‐ranged species on geologically young islands postulates that nonequilibrium communities here have a higher speciation rate owning to frequent habitat disturbance by, among others, volcanic activity, cyclones, and landslides (Whittaker, 2000). Finally, the physiological preference of different taxonomic groups probably accounts for their distinctively elevational richness along the same gradient (Krömer et al., 2013; Krömer et al., 2005; Rahbek, 1995).

Epiphyte salient features

Without access to a buffering supply of water and nutrients in the forest soil, the arboreal habitat for epiphytes is extremely dynamic in terms of moisture and nutrient availability. Accordingly, epiphytic plants have evolved morphologically and physiologically to deal with the typical water and nutrient‐stress conditions in the forest canopy. Bromeliads form a good example to illustrate how epiphytic plants have adapted to their arboreal habitat. Many bromeliads have developed a rosette growth form that serves as a reservoir for water and litter. Uptake is facilitated by the presence of specialized structures (trichomes) on the leaf surface. Moreover, many bromeliads possess a water‐saving metabolic pathway (Crassulacean Acid

Metabolism, CAM). To reduce evapotranspiration during the day, CAM plants acquire CO2 mostly at night, and the pre‐collected CO2 is stored as an intermediate product of malic acid in special water storage tissue that permits this two‐step carbohydrate fixation process. CAM presumably evolved as an adaptation to arid conditions. CAM occurs in about 4% of the vascular flora and a majority is epiphytic plants, such as bromeliads (Martin, 1994; Winter and Smith, 1996). Interestingly, CAM plants are also found in aquatic environments, extremely wet forests or shaded understory in (sub‐)tropical areas (Pierce et al., 2002; Craig, 2005; Skillman and Winter, 1997). This has led to the speculation that CAM might have evolved in response to CO2 availability instead of drought stress (Benzing, 1990; Keeley, 1996).

Epiphytic bromeliads occur exclusively in the Neotropics. In the paleotropical area, a similar niche is apparently occupied by the widespread Asplenium species, the ‘bird’s nest fern’. The nickname bird’s nest is derived from its rosette growth form, which traps fallen leaves and

CHAPTER 1 other debris. The clumped plant bases are composed of fibrous roots and trapped humus, which sponge up rainwater to facilitate successful establishment in the forest canopy. Adult plants may reach 300 cm in diameter, creating conspicuous populations in the forest canopy. The genetic differentiation in bird's nest ferns such as Asplenium antiquum at the large spatial scale of East Asia is high (Murakami et al., 1999). However, regional variation for species such as A. nidus may also be high and presumably leads to many cryptic species (Zhang et al., 2010).

Epiphytes in a changing environment

The steep latitudinal gradient of epiphyte distributions shows that most epiphyte species occur in (sub‐)tropical areas. Compared with temperate species, tropical species experience limited annual thermal variability and the thereby resulting thermal specialization might render tropical species amongst the most imperilled species on Earth due to global warming (Laurance et al., 2011; Cunningham and Read, 2003). Physiologically, a rising temperature may directly alter the metabolic and evaporation rates of plants. For instance, non‐vascular epiphytes in tropical mountains show an optimum photosynthetic rate at mean habitat temperature, suggesting an adaptation to the local thermal regime (Wagner et al., 2013). A rising temperature might increase the evaporation rate, causing dehydration and carbon loss. Under manipulated warming conditions, epiphytic orchids also showed a reduction in biomass, by 30%, and a shortening of the flower spikes (Vaz et al., 2004). Notably, the warming trend is more pronounced at night, leading to a decrease of the diurnal temperature range (Solomon et al., 2007). For CAM species, a small change above the nightly temperature optimum would decrease air humidity, and in turn markedly reduce stomatal conductance and the amount of

CO2 available for the synthesis of malic acid, which may cause carbon loss (Martin, 1994).

On the other hand, atmospheric CO2 has been expected to exceed 550 ppm by the second half of this century, a doubling of the preindustrial concentration of 280 ppm (Solomon et al., 2007). Since the photosynthesis rate is not carbon saturated under current atmospheric CO2 level, plants may uptake more carbon under increased ambient CO2 concentration which leads to a faster growth (Körner, 2000). However, response of plants to elevated CO2 does not merely depend on assimilation rate, water‐use efficiency is also crucial. The slow‐growth CAM plant demonstrates the trade‐off between water transpiration and biomass accumulation. In addition, even desiccation tolerant plants (bryophytes and lichens) show a long‐term reduced photosynthesis in response to elevated CO2, and the short‐term positive reaction is relatively small and taxon‐specific (Tuba et al., 1999; Monteiro et al., 2008).

Some future climate change scenarios project an increase in annual rainfall and in the number of dry days, which might increase the frequency and/or intensity of extreme weather events (e.g. floods, drought; Solomon et al., 2007). Water availability is a determining factor for

INTRODUCTION epiphyte distribution (Gentry and Dodson, 1987a), yet rainfall seasonality rather than total rainfall is more relevant to epiphyte survival (Zotz and Hietz, 2001). Hence, the redistribution of seasonal rainfall under climate change might have a bigger influence on epiphytes than an increased rainfall.

Another important source of water for epiphytes, the so‐called horizontal precipitation (i.e. fog/cloud water), has also been projected to change due to global warming. Rising sea surface temperatures presumably would cause a lifting of the cloud base, thereby decreasing ground‐level clouds. A decrease in the frequency of cloud immersions may threaten the survival of tropical montane cloud forests (TMCF, Still et al., 1999). TMCF, estimated to represent about 14.2% of all tropical forests, are characterized by a conspicuous epiphyte community, contributing up to 35% of the floristic diversity and up to 60% of total abundance (Gentry and Dodson, 1987a; Wolf and Flamenco‐S, 2003; Mulligan, 2010). Under continuously high air humidity, many TMCF epiphytes are poikilohydric (e.g. bryophytes, Hymenophyllaceae, Grammitidaceae) that react strongly to humidity change. Epiphytes intercept a disproportional high amount of rainfall and cloud droplets in view of their contribution to total forest biomass, and thus epiphytes may have a relatively large influence on the hydrology and nutrient cycles of TMCF (Hofstede et al., 1993; Hsu et al., 2002; Pypker et al., 2006). A dieback of TMCF epiphytes would not only affect the hydrological cycle, but also have a negative impact on associated fauna (e.g. canopy amphibians), leading a possible cascading effect in this unique ecosystem (Benzing, 1998; Foster, 2001). Since the level of endemism in TMCF is high, presumably due to geographical isolation and narrow climatic conditions, the loss of TMCF species is especially detrimental (Ponce-Reyes et al., 2013; Leo, 1995).

Occupying the most climate‐defined space in the forest, epiphytes are often assumed to be more sensitive to atmospheric change than the soil‐based flora. Non‐vascular epiphytes, such as lichens and bryophytes, have long been used as indicators for air pollution and acid rain (Farmer et al., 1992; Szczepaniak and Biziuk, 2003). Therefore, it is not surprising that ecologists have been aware of the potential of epiphytes for monitoring anthropogenic climate change (Lugo and Scatena, 1992). In response to the warming climate of the past two decades, several (sub‐)tropical epiphytic bryophytes and lichens species have invaded Europe (Frahm, 2001; van Herk et al., 2002). However, up to now, little physiological and ecological information is available for vascular epiphytes to predict their likely response to on‐going global climatic change.

CHAPTER 1

Simulating species responses to climate change

The survival risk from climate change varies amongst biomes and, similarly, the response to climate change is also species‐specific (Thomas et al., 2004; Loarie et al., 2009). Species responses to changing environments include migration, genetic adaptation and tolerance (phenotypic plasticity). If the intensity and velocity of change is beyond the ability of a species to cope, extinction is inevitable. Therefore, the ability of dispersal and establishment may well determine the vulnerability of a species to climate change, and so is the extent of species genetic adaptation (Hedderson and Longton 2008). Widespread (generalist) species that occur across a broad range of environmental gradients, comprising several climatically‐adapted populations, may be less vulnerable since the ability of these species to occupy diverse habitats may permit populations to persist in spatially and temporally changing environments (Silander 1985). Therefore, generalist species are likely to demonstrate broader tolerances to climate change than specialists that are geographically restricted (Broennimann et al. 2006; Aitken et al. 2008). Accordingly, the range size of a species might be an indicator to assess species vulnerability to climate change. Furthermore, the altitudinal range of a species in mountain areas might be interpreted as the degree of thermal specialization (Janzen, 1967; Huey, 1978). To evaluate species sensitivity to manipulated climate‐change conditions, in vitro experiments or in situ reciprocal transplant field experiments may be used (Nadkarni and Solano 2002; Vaz et al., 2004; Song et al. 2012). For epiphytes, field studies on the adaptability to simulated conditions of climate change are still rare.

In field experiments, warming conditions may be simulated by transplanting species to lower latitudes or elevations. These studies, however, are logistically complex and time consuming, which is one of the reasons why species distribution models (SDMs) are increasingly used to estimate the potential range shift of species under future climate change conditions (Bakkenes et al., 2002; Broennimann et al., 2006; Hijmans and Graham, 2006; Thuiller et al., 2006; Carnaval and Moritz, 2008; Fitzpatrick et al., 2008; Jensen et al., 2008). SDMs attempt to recognize species’ realized niche by relating species occurrences with values of predictor variables across a series of observation sites (Guisan and Thuiller, 2005). This modelling‐based approach provides valuable first‐order assessments of potential climatic change impacts on biodiversity (Huntley et al., 2010). Another advantage of SDMs is the visualization of the predicted distribution of each species, cumulating in an one‐picture overview to demonstrate regional patterns.

Notwithstanding the general acceptance of SDM’s as a valuable tool, several aspects of purely climate‐based models have been criticized (Heikkinen et al., 2006; Austin and Van Niel, 2011). For example, SDMs tend to overestimate the area of suitable habitats, particularly for those species with a strong dependency on other species, such as epiphytic plants (Huntley

INTRODUCTION et al., 2010). Epiphyte distribution relies on the presence and characteristics of host trees. Precisely, it is the composition of and structure of the host trees in a forest that significantly influence epiphyte assemblages, which might be attributed to the microclimate associated with forest types (Benavides, 2010). Numerous studies have indicated the importance of incorporating biotic interactions for improving the accuracy of SDMs (Leathwick et al., 1996; Araújo and Luoto, 2007; Preston et al., 2008). Another criticism to climate SDM’s is that the velocity of climate change often outpaces the migration capacity of many species (Svenning et al., 2008; Thuiller et al., 2008). Therefore, it is crucial to take dispersal limitation into account when simulating species distributions (Engler and Guisan, 2009). However, because it is difficult to obtain reliable dispersal data, most studies assume either unlimited or no dispersal for the target species. Other debates concern species persistence under unfavourable climatic conditions (Loehle and LeBlanc, 1996). Common sense dictates that many species, especially long‐lived trees, will not immediately perish after climate changes and this justifies including species persistence in SDM’s. Finally, a general shortcoming of SDM’s is the disregard for intraspecific variation in the modelled species. Many species are projected to tolerate climate change better when sub‐taxon information is considered (Pearman et al. 2010; Benito Garzón et al. 2011; Oney et al. 2013).

Study Area

Taiwan (formerly known as Formosa) is a continental island, separated from Southeast China by the ca. 200 km wide Taiwan Strait. With an area of 36,000 km2, the Tropic of Cancer crosses through the middle of the southern half of the island (Chapter7; Fig. 1). Taiwan owes its existence to a collision of the Philippines Sea plate with the Eurasian continental margin some five million years ago (Ho, 1988). Subsequent active orogenesis promoted the creation of an extensive mountain system on the island; about 70% of the area is covered by (> 1,000 m asl) mountains. Mt. Jade (3952 m) is the highest peak within the more than 50 peaks above 3,000 m asl in Taiwan.

There is no distinct dry season in Taiwan. Unlike most areas at the tropic of Cancer or Capricorn that are relatively arid, Taiwan has a humid climate thanks to the high mountains that induce cloud formation from high‐humidity oceanic winds. The annual rainfall ranges from 1,000 mm to over 6,000 mm, and generally falls during the NE monsoon (October– January), spring rain (February–April), plum rain (May–June) and typhoon‐induced heavy rain events (July–September). The NE monsoon accounts for 45% of the total annual rainfall, mainly in east Taiwan (Kao et al., 2004). On average, 3.7 typhoons hit Taiwan in summer (July to September) each year, of which about 80% land on the east coast with westbound tracks (Wu and Kuo, 1999). The dominating central range on the island often has a complex interaction with the typhoon circulation and could decrease the intensity of typhoons by an

CHAPTER 1 average of over 40% within 12h after the storm centre reaches the island (Wu and Kuo, 1999). Therefore, the western part of the island on the lee side of the central range receives less impact from typhoons.

Taiwan floristic diversity is high, comprising ca. 4077 species (Hsieh, 2003). The dramatic biodiversity is driven by habitat heterogeneity and the diversity in biomes on this island, ranging from alpine tundra to tropical rain forests. In addition, the (sub‐)tropical location enables Taiwan to receive tropical and temperate species from adjacent regions; for example, ca. 25% of the pteridophyte flora consists of “marginal species” (i.e. tropical or temperate species at their northern or southern limit of the geographical distribution, respectively, Moore, 2000). Finally, the oceanic climate facilitated Taiwan as a refuge during Quaternary glaciations, a presumable explanation for the high number of epiphytic species in Taiwan. Tropical islands provide an ideally natural laboratory for testing ecological and evolutional theories, for their compressed biodiversity and simplified ecosystem within a relatively small land area. The mountainous island of Taiwan is therefore a well‐located site for describing distribution patterns and testing corresponding hypotheses.

Aims and contents of this thesis

The overall goal of this thesis is to get insight in the relative vulnerability of epiphytic species and associated forest types of Taiwan to global climate change. To achieve this goal, descriptive, experimental (laboratory and field), and modelling approaches are all applied.

Chapter 2 is a descriptive study of the epiphyte flora of Taiwan. After consultation of the herbarium specimens and own field observations, for the first time, a checklist of the vascular epiphytes in Taiwan and several associated islets is organised. The systematic composition of the epiphyte flora of Taiwan and its phytogeographical connection with adjacent areas is described and explanations are proposed.

Chapter 3 is also largely descriptive. Thanks to the wealth of information available in herbarium collections and published literature, an epiphyte database is compiled, comprising ca. 39,000 unique records. Based on the assembled collections, regional and altitudinal patterns of epiphyte distribution are described in more detail. Altitudinal richness patterns are tested with the mid‐domain effect theory. Next, a species distribution modelling (SDM) approach, MaxEnt, is used to obtain a more complete picture for the distribution of species, and a summarizing richness map is constructed. The relative importance of environmental factors for epiphyte distribution is furthermore explored with ordination analysis (canonical correspondence analysis). Special attention is paid to the influence of typhoons on epiphytes and the altitudinal distribution of thermal specialists for the reason that thermal specialist may be more vulnerable to global warming.

INTRODUCTION

In chapter 4, the influence of environmental factors on epiphytes is further evaluated in both field and laboratory experiments that focus on the uptake of atmospheric CO2 by the CAM epiphyte Hoya carnosa. Diurnal acid accumulation and leaf carbon isotope are compared between dense and open forests to evaluate the effect of increased CO2 availability.

Chapter 5 is another ecophysiological study. Using a common bird's nest fern, Asplenium nidus, the photosynthetic rates of its leaf blades that receive different levels of sunlight on both surfaces are compared to assess the photosynthetic plasticity of the epiphytic fern in relation to microclimate variation.

In Chapter 6, another species of bird's nest fern, Asplenium antiquum, is studied in the field to understand the intraspecific variation of this altitudinally widespread epiphytic fern in response to climate change. Climate change is simulated by reciprocally transplanting individuals between high (1950 m asl), mid (1100 m asl) and low (600 m asl) elevations. Mortality and growth rates of transplanted juvenile plants are monitored over two years.

Finally, in chapter 7 again a SDM modelling approach is used to assess climate change impacts on forests and epiphytes in Taiwan. Here, a novel hierarchical model, tailored for epiphytes was developed by incorporating dispersal limitation, tree persistence, and non‐climatic factors and by considering biotic interactions between epiphytes and host trees. The model is used to identify certain forest types and species that are relatively more sensitive to projected scenarios of climate change. For identified areas that fall outside current conservation reserves and with a relatively high number of vulnerable species, additional human disturbance is likely to exacerbate the effect of climate change, thus deserving prioritised conservation measures.

Chapter 2 Diversity and phytogeography of vascular epiphytes in a tropical‐subtropical transition island, Taiwan

The Taiwanese epiphyte flora is dominated by Pteridophytes (i.e. ferns and fern allies, 171 spp.) followed by orchids (120 spp.). CHAPTER 2

Diversity and phytogeography of vascular epiphytes in a tropical-subtropical transition island, Taiwan

Rebecca C.-C. Hsu & Jan H. D. Wolf

Flora 204, no. 8 (2009): 612-627

Abstract

We present the first checklist of vascular epiphytes in Taiwan, based on herbarium specimens, literature records and field observations. Epiphyte phytogeography was analyzed using Takhtajan’s modified division in floristic regions. We ascertain the presence of 336 species of vascular epiphytes (24 families, 105 genera) in Taiwan. Pteridophytes contribute most species (171 species), followed by orchids (120 species). Epiphytes contribute eight percent to Taiwanese floristic diversity and epiphyte endemism is near 21.3%. The extensive mountain system is probably the most effective driver for epiphyte diversification and endemicity in Taiwan. Phytogeographically, Taiwanese epiphytes exhibit equal affinity to the Malesian region, southern China and Indo-China, and Eastern Asiatic regions. However, some species have a disjunctive distribution between Taiwan and SW China and/ or E Himalaya, presumably related to low habitat similarity with adjacent China and/or the legacy of Late Quaternary climate change. Vascular epiphyte distribution patterns corroborate the phytogeographical separation of the island of Lanyu from the main island of Taiwan along Kanto’s Neo-Wallace Line.

Introduction

The conspicuous vascular epiphyte community in the canopy of wet tropical forests has attracted botanists as early as 1888, especially during the second half of the last century (Benzing, 1990; Gentry and Dodson, 1987a; Johansson, 1974; Kress, 1986; Madison, 1977; Richards, 1952). These studies have shown that the epiphytic life-form is a successful adaptation of plants to conditions in the canopy, comprising ca. 29,000 species, or approximately 10% of all vascular plants, in 83 different families and 876 genera (Gentry and Dodson, 1987a). Whereas the number of epiphyte inventories is gradually increasing, inventories from the paleotropics are still rare and especially from Asia few inventories are available (Wolf and Flamenco-S, 2003). In addition, little is known about epiphytes in tropical- subtropical transition zones. Consequently, the differences in vascular epiphyte diversity and

EPIPHYTE DIVERSITY AND PHYTOGEOGRAPHY composition between temperate and tropical areas and between paleotropics and neotropics remain ambiguous and lack generally accepted explanations (Benzing, 1987; Gentry and Dodson, 1987a; Zotz, 2005).

Fig. 1 Location of Taiwan, Lanyu, Lutao, and the Neo‐Wallace Line (Kanto 1993)

CHAPTER 2

Taiwan (formerly known as Formosa) is a continental island, separated from Southeast China by the ca. 200 km wide Taiwan Strait, which reaches a depth of 70 meters. The Tropic of Cancer crosses through the middle of the southern half of the island, and about 70% of the total area is covered by mountains. Taiwan owes its existence to a collision of the Philippines Sea plate with the Eurasian continental margin some five million years ago, which induced orogenesis (Ho, 1988). In contrast to many other regions at the tropic of Cancer or Capricorn, Taiwan has a humid climate thanks to the high mountains that induce cloud formation in high-humidity oceanic winds. Frequent typhoons in summer and NE monsoon in winter provide most precipitation throughout the year.

Taiwan floristic diversity is high, comprising ca. 4077 species (Hsieh, 2003). Being a mountainous island, species diversity is the result of great habitat heterogeneity. Furthermore, situated at the transition from tropics to subtropics, in Taiwan many tropical plant species reach their northern limit (Hsueh and Lee, 2000), whereas temperate species are found in the high mountains (Hosokawa, 1958). Phytogeographically, Taiwan belongs to the Eastern Asiatic region (Takhtajan, 1986). Yet the south end of Taiwan, Henchun Peninsula, and two small volcanic islands, Lanyu and Lutao, located in the south-eastern Taiwan, are pertained to Malesian region (Fig. 1, Fig. 2). The vegetation of Lanyu is characterized by tropical rain forests, and its flora and fauna have more in common with the Philippines than with Taiwan. On this basis, Kanto (1933) proposed the Neo-Wallace Line by extending the boundary of Dickerson and Merrill’s Line (Dickerson, 1928) from northern Luzon to Lanyu through the middle sea of Lanyu and Lutao (Fig. 1). Kanto’s proposal was corroborated by several subsequent biogeological studies (Hosokawa, 1958; Kanehira, 1935; Yen et al., 2003).

In this study we describe the epiphyte flora of Taiwan for the first time. Specifically, we address the following research questions: (i) is species richness, endemism, and familial makeup similar to that of other floristic regions such as tropical and temperate areas in the neotropics, (ii) what is the phytogeographical affinity of epiphytes and several sub-categories, (iii) do epiphytes corroborate the Neo-Wallace Line?

Materials and Methods

Study Site

Taiwan is situated between 21˚45'-25˚56'N and 119˚18'E-124˚34'E with an area of 36,000 km2 (Fig. 1). The Central Ridge of Taiwan comprises over 200 peaks higher than 3000 meters asl, and Yushan is the highest (3952 m) peak in this island. The annual rainfall ranges from 1000 to over 6000 mm (data from 1949-2004). Mean monthly temperature in the lowlands ranges from 15 to 20Ԩ, and is about 28Ԩ in summer. Based on bioclimatic analyses, Taiwan can be classified into seven climatic regions, and Lanyu is separated independently (Su, 1984, 1992).

EPIPHYTE DIVERSITY AND PHYTOGEOGRAPHY

Lanyu (ca. 46 km2, also known as Botel Tobago, Kotosho, and Orchid I.) and Lutao (ca. 16 km2, Green I., Kwasyoto I., and Samasana I.) are small tropical islands located at 22˚03’N, 121˚32’E and 22˚40N, 121˚29E, respectively. During summer and early autumn, typhoons frequently hit Taiwan, which have less impact in western Taiwan, sheltered by the Central Ridge.

Fig. 2 Takhtajan’s floristic regions. Numbers indicated: 2, Eastern Asiatic region; 2‐20, Ryukyu islands; 2‐25, SW China; 2‐27, E Himalaya; 12, Sudano‐Zambezian region; 15, Madagascan regions; 16, Indian region; 17, Indochinese region; 18, Malesian region; 18‐104, Philippines; 19, Fijian region; 20, Polynesian region; 22, Neocaledonian region; 29, NE Australian region. Regions that not covered in above map but with Taiwanese epiphyte occurrence are: 3, North American Atlantic region; 4, Rocky Mountain region; 6, Mediterranean region; 8, Iran‐Turanian region; 9, Madrean region; 10, Guineo‐Congolian region; 21, Hawaiian region; 23, Caribbean region; 24, Guayana Highlands; 25, Amazonian region; 26, Brazilian region; 27, Andean region. The figure was modified from Takhtajan (1986).

CHAPTER 2

Epiphyte definition

We define epiphytes as organisms that grow on plants without extracting water or nutrients from hosts’ living tissues, following Barkman (1958). In this paper, focus is on vascular plants, but many other epiphytic organisms are found in the canopy of the forest. In addition, it is not rare to find accidental epiphytes growing on other plants, which are unable to reproduce in the canopy (Moffett, 2000). We excluded accidental epiphytes from our checklist and classified vascular epiphytes in following sub-categories: i. Holo-epiphytes: epiphytes that complete their entire life cycle without contacting the forest floor (Benzing, 1990). ii. Hemi-epiphytes: epiphytes that complete part of their life cycle as terrestrial plants. Primary hemi-epiphytes begin their life cycle as epiphytes and eventually send their roots to the ground (e.g. strangler figs), whereas secondary hemi-epiphyte seedlings germinate terrestrially to become epiphytic secondarily when their rooting shoots decompose (e.g. aroids). iii. Facultative epiphytes: species in which some individuals are terrestrial.

Epiphyte checklist

Botanically, Taiwan is one of the best explored regions in the tropics. The national database houses over 200,000 botanical records (ca. 60% of herbarium collections). We gratefully made use of this wealth of information, scrutinizing for epiphytes in well-known epiphytic taxonomic groups (Benzing, 1990). In addition, we used epiphyte records in published plant inventories and floras. Nomenclature follows the 2nd edition of the Flora of Taiwan (Boufford et al., 2003). To compile this checklist, species listed in Flora of Taiwan were examined one by one, and the approximate number of epiphytes was ascertained.

Phytogeography analyses

We assessed the presence of Taiwanese vascular epiphytes in Takhtajan’s floristic regions (Takhtajan, 1986). The floristic provinces, SW China, E Himalaya, Ryukyu and Philippines under Eastern Asiatic and Malesian regions of Takhtajan’s system, were recognized independently (Fig. 2). Species geographical distributions were consulted flora of Taiwan and collections in the global biodiversity information facility (GBIF) online database. For smaller floristic provinces, such as SW China and Ryukyu, the floras of Japan and China were consulted to determine the specific occurrence locations.

EPIPHYTE DIVERSITY AND PHYTOGEOGRAPHY

Table 1 Contribution of vascular epiphytes to the flora of Taiwan in various taxonomic categories (data Flora of Taiwan, Boufford et al., 2003).

All vascular Ferns & allies Angiosperm Dicotyledons Monocotyledons plants

Families 24/235(10%) 12/37(32%) 12/190(6%) 10/151(7%) 2/39(5%) Genera 105/1419(7%) 48/145(33%) 57/1257(5%) 16/901(2%) 41/356(12%) Species 336/4077(8%)* 171/629(27%) 165/3420(5%) 40/2410(2%) 125/1010(12%)

*Epiphyte‐Quotient

Results

Species richness, family makeup, and endemism

There are 336 species of vascular epiphytes in 105 genera and 24 families in Taiwan and two subsidiary isles, Lanyu and Lutao (Appendix 1). Obligate holo-epiphytes comprise 271 (81%) species, 41 (12%) species are facultative holo-epiphytes, and 7 (2%) and 17 (5%) species are primary and secondary hemi-epiphytes, respectively.

The Taiwanese epiphyte flora is dominated by Pteridophytes, i.e. ferns and fern allies, comprising 171 species (Table 1). The number of orchids is also substantial, 120 species (Fig. 3). The ten most species-rich families contain 89% of all epiphytes and the remaining plant families with epiphytic representatives only contribute about 11% to total epiphyte richness (Fig. 3). At the genus level also, epiphytism is concentrated in few taxa. Only five percent of the genera contain more than 10 species and 54 (51%) genera are represented with a single species only in the region. More than a quarter of native Pteridophytes (Table 1) and 36% of native orchids are epiphytes. In contrast, the Epiphyte-Quotient (Ep.-Q, Hosokawa, 1950), i.e. the proportion of epiphytic species in the flora, is only approximately 8% (Table 1).

Of the 336 epiphytes, 75 are endemic species. Sixty-nine species are confined to Taiwan, and one disjunctively occurs in Taiwan and Lanyu. Despite the small size of Lanyu and Lutao, 5 species are confined here (4 species are endemic to Lanyu, and one species is shared by both). The proportion of Taiwan endemic epiphytes (21.3 %, Table 2) is less than that in the entire flora (26.2 %, Hsieh, 2003). Most endemic epiphytes are orchids (54.2 %) despite overall higher number of epiphytic Pteridophytes in Taiwan. Of all 114 epiphytic orchids, 38 species (33.3%) are endemic to Taiwan, as opposed to 19 species (11.2%) of Pteridophytes (Table 2).

CHAPTER 2

Table 2 Floristic affinity of Taiwan epiphyte flora with phytogeographical regions, following Takhtajan (1986). Given is the proportion (%) and number of Taiwanese species, in parentheses, of epiphytic Taiwanese species per region.

Floristic Regions Taiwan Lanyu Lutao Pteridophytes Orchids (324) (69) (25) (170) (114)

Eastern Asiatic Region 38.9 (126) 50.7 (35) 64.0 (16) 48.8 (83) 25.4 (29)

China, Japan, Korea 27.2 (88) 21.7 (15) 40.0 (10) 31.2 (53) 20.2 (23)

E. Himalaya & S.W. China 13.0 (42) 4.4 (3) 0.0 (0) 13.5 (23) 13.2 (15)

Ryukyu 13.0 (42) 29.0 (20) 24.0 (6) 18.2 (31) 6.1 (7)

Malesian Region 40.9 (132) 71.0 (49) 72.0 (18) 51.8 (88) 25.4 (29)

Malay archipelago 31.2 (101) 49.3 (34) 64.0 (16) 42.4 (72) 14.0 (16)

Philippines 9.6 (31) 21.7 (15) 8.0 (2) 9.4 (16) 11.4 (13)

Indo‐China 39.2 (127) 46.4 (32) 60.0 (15) 43.5 (74) 35.1 (40)

India & Sirilanka 23.5 (76) 29.0 (20) 52.0 (13) 28.8 (49) 14.9 (17)

Melanesia & Hawaii 12.0 (39) 26.1 (18) 44.0 (11) 20.0 (34) 1.8 (2)

Africa 4.9 (16) 8.7 (6) 8.0 (2) 7.1 (12) 0.9 (1)

Australia 9.0 (29) 18.8 (13) 36.0 (9) 12.4 (21) 1.8 (2)

Neotropis 2.5 (8) 5.8 (4) 4.0 (1) 3.5 (6) 0.0 (0)

Holarctis other than E.A. 1.5 (5) 2.9 (2) 0.0 (0) 2.9 (5) 0.0 (0)

Endemicity 21.3 (69) 5.8 (4) 0.0 (0) 11.2 (19) 33.3 (38)

EPIPHYTE DIVERSITY AND PHYTOGEOGRAPHY

Epiphyte phytogeography

With respect to phytogeographical region, about 41% of epiphytes in Taiwan also occur in the Malesian region, including 10% of species shared with only the Philippines (Table 2). About 39% of species are shared with Indo-China, and about the same proportion is shared with Eastern Asiatic regions, which cover temperate E Asia, E Himalaya, SW China, and Ryukyu. The islands Lutao and Lanyu share most species (over 70%) with the Malesian region, whilst Lutao has a high proportion (40%) of species that also occur in temperate E Asia. Only Lanyu shares an exceptional high proportion (22%) of species with the Philippines (Table 2).

Overall, epiphytic ferns shared more species with other floristic regions than total epiphytic species (Table 2). Over forty percent of Taiwanese epiphytic ferns also occurred in Eastern Asiatic, Malesian, and Indochinese regions. Epiphytic orchids exhibited the highest affinity (35%) to Indo-China, yet shared no species with Neotropical and Holarctic areas, except E. Asia.

Fig. 3 Ten most species‐rich epiphytic families and their contribution to total epiphyte flora in Taiwan. Numbers in parentheses are species numbers. Shading indicates Pteridophyta.

CHAPTER 2

Discussion

Species richness and taxonomic distribution

For a paleotropical region, the island of Taiwan is with 336 species rich in epiphytes (Table 1). There is no distinct dry season in Taiwan and abundant rainfall and warm climate promote epiphyte species richness and growth. Another reason why epiphyte richness is high may be that Taiwan served as a refuge during Late Quaternary climate change, which has been used to explain the exceptionally high diversity in Taiwan (4077 plant species; further discussed below). In view of this high floristic diversity, Taiwan may even be considered relatively poor in vascular epiphytes. The contribution of vascular epiphytes to total vascular flora is only eight percent, whilst the EP.-Q worldwide is near ten percent. Moreover, about 36% of orchids are epiphytic in Taiwan, which is far less than the 70% worldwide level (Atwood 1986). Possibly frequent tropical storms have reduced epiphyte diversity in Taiwan. On average, five typhoons hit Taiwan each year (data from 1958 to 2007, Central Weather Bureau). Typhoons may have a dramatic impact on forest canopies and cause understory light levels to increase to 30% of outside levels (Lin et al., 2003). Similarly, low epiphyte diversity in Puerto Rico has been attributed to island isolation and large-scale hurricane disturbances (Migenis and Ackerman, 1993).

Epiphyte richness in neotropical areas, moreover, is generally higher. For example, Wolf and Flamenco-S (2003) report 1173 species for the state of Chiapas (75,000 km2, 16- 18˚N). Typical for any epiphyte flora, the diversity is concentrated in few taxa (Fig. 3, Table 1). In contrast to the Neotropics, paleotropical areas lack particularly species-rich epiphyte families (e.g. Bromeliaceae, Cactaceae and Marcgraviaceae) and genera in the orchids (e.g. Pleurothallis, 1500 spp.; Epidendrum, 720 spp.; Maxillaria, 570 spp.; Stelis, 540 spp.) and in the aroids (Anthurium 600 spp.; Philodendron (350 spp.) (Benzing, 1990). In Taiwan, the most abundant epiphytes are ferns, and in this respect Taiwanese epiphyte flora is typical for temperate regions. However, in comparison with other vegetation types, ecosystems, and floristic regions, the relative proportion of epiphytic ferns and orchids of Taiwan is not dramatically different, showing a transition from tropical to temperate regions (Table 3). A high proportion of ferns and fern allies is probably due to the presence of temperate mountains in Taiwan that favour epiphytic ferns over, for example, orchids (Kessler et al., 2001, Zotz, 2005). In Taiwan, no epiphytic orchids are found above approximately 2300 meters asl (Gastrochilus hoii, pers. comm.) in contrast to epiphytic ferns with ultimate altitudes of ca. 3000 meters asl (e.g. Pyrrosia spp., Lepisorus spp., Mecodium wrightii, pers. observ.).

EPIPHYTE DIVERSITY AND PHYTOGEOGRAPHY

Epiphyte endemism

Many islands are considered global biodiversity hotspots because of high endemicity of insular biota (Kreft et al., 2008). Taiwan is no exception, having extraordinary plant endemicity. More than one thousand vascular plant species are endemic to the island, comprising 26% of the entire flora. The strikingly high flora endemism can be explained by Taiwan’s extensive mountain system. Taiwan was formed from the collision between the Philippines Sea plate and the Eurasian continental margin and gave rise to the Central Ridge of Taiwan in the Mid Pliocene (3 Ma) (Ho, 1988). Active orogenesis induced a massive earthquake in central Taiwan as recent as 1999. Orogenesis results in greater microhabitat differentiation of mountainous regions, which promotes island-wide biodiversity and endemicity. Kreft et al. (2008) concluded that in continental islands, geographic isolation from the mainland may contribute less to species diversity than mountain isolation. Our data are in agreement with this conclusion. For example, several epiphytic genera of mountainous regions, Bulbophyllum (24 spp.), Gastrochilus (9 spp.) and Oberonia (7 spp.), show exceptionally high endemicity of nearly 50 percent. Furthermore, Goodyera, a mid-elevation (ca. 1500-2000 m asl) species, evolved three epiphytic species, including two endemics. This is the first report of epiphytism in this genus. Finally, endemicity increases with altitude in Taiwan up to nearly 60% above 3500 meters asl

Yet, vascular epiphytes show lower endemism (21.3%) than terrestrial plants (Table 2). This may be due to their superior dispersal ability; 89 percent of vascular epiphytes in Taiwan disperse by wind. The arboreal habitat and dust-like seeds and diaspores enable long- distance dispersal. Overall, ferns show wider ranges and lower endemicity than angiosperms (Gentry and Dodson, 1987a; Kelly et al., 2004) (Table 2). In contrast with epiphytic seed plants, most large epiphytic fern genera are preponderantly pantropical (Gentry and Dodson, 1987a). Apart from dispersal ability, historical factors may also explain species geographical range (Lester et al., 2007). Kelly et al. (2004) reported that in the tropical Andes species endemism increased from primitive to advanced taxonomic groups (bryophytes < Pteridophytes < angiosperms). Furthermore, taxa with narrow geographical range are often considered to have high speciation rates (Kelly et al., 2004). In this view, the high endemism (33%) in Taiwanese epiphytic orchids in Taiwan relates to their highly specific pollination system, which, together with the fragmented canopy habitat, promotes rapid speciation (Benzing, 1987; Gentry, 1982; Gentry and Dodson, 1987a; Gravendeel et al., 2004).

Epiphyte phytogeography

Taiwan has a relatively unique vascular epiphyte flora. The regions with closest affinity are the Malesian region, Indo-China, and Eastern Asiatic regions; ca. 40% of Taiwanese species are shared with those regions. Interestingly, about 13% of vascular epiphytes have a disjunctive distribution between Taiwan and SW China and/or E Himalayan regions (Table 2). This

CHAPTER 2 floristic disjunction is consistent with Hosokawa’s (1958) finding that Taiwan’s flora, especially of the highland, is more closely related to SW China and E Himalaya than to adjacent coastal provinces of mainland China. Kuo (1985) indicated similar observations on Taiwanese Pteridophyte flora. He found that the Pteridophytes of warm-temperate forests (500 to 1800 meters asl) were closely related to SW China and the Himalayan regions, whilst lowland species showed higher affinity to Ryukyu, south-eastern China and Indo-China.

The simplest explanation for the lower epiphyte affinity of Taiwan with adjacent coastal regions of south-eastern China is lack of suitable habitats (Kuo, 1985). Due to long term population pressure and associated agricultural activities, south-eastern China has endured extensive habitat change. Since epiphytes are most diverse and abundant in old- growth forests (Cascante-Marin et al., 2006; Köhler et al., 2007; Wolf, 2005), epiphyte diversity is especially affected. Furthermore, lowland south-eastern China shows little habitat similarity with Taiwan mountain areas.

Late Quaternary climate change offers another explanation. On an evolutionary time- scale, epiphytism is relatively recent, occurring in evolutionary advanced families of ferns and seed plants. Orchidaceae did not evolve until the Quaternary (1.6 Ma ago) (Benzing, 1990). Zotz (2005) discussed the possibility that the Pleistocene extinction was one of the limits of epiphytism in temperate zones, whilst few temperate areas (e.g. Chile, New Zealand, Himalayas, Japan) have a high number of epiphytes for being Tertiary refugia. The common feature of the flora in these areas is a high proportion of autochthonous and monotypic taxa. During the ice age in the Quaternary, the sea level in the Taiwan Strait dropped, connecting Taiwan with mainland Eurasia. According to the projected vegetation map of Last Glacial Maximum (LGM, 18,000 ago), Eurasia had relatively scarce tree cover with scattered areas of close forests in the uplands across south-western China and along the south-eastern coast of Eurasia (Ray and Adams, 2001). Presumably, the oceanic climate facilitated Taiwan as a refuge during Quaternary glaciations. Moreover, apart from high endemicity, more than half of plant genera in Taiwan are monotypic (Hsieh, 2003). There is an endemic monotypic epiphyte genus Haraella (Orchidaceae) in Taiwan. Thus, we propose that Late Quaternary climate change helps explain the disjunctive distribution of many vascular epiphytes between Taiwan and south- western China as well as eastern Himalayan regions.

Interestingly, the epiphyte flora of Lanyu and Lutao is phytogeographically distinct. Lanyu has more affinity with the Philippines (22%) in the Malesian region than Lutao (8%), whereas Lutao shares more species with China, Japan and Korea in the Eastern Asiatic Region (40%) than Lanyu (22%) (Table 2). This pattern is in agreement with the proposed Neo- Wallace Line based on insect distributions (Kanto, 1933).

EPIPHYTE DIVERSITY AND PHYTOGEOGRAPHY

In summary, this one of the few epiphyte inventories in Asia shows that the Taiwanese epiphyte flora is rich in species and has an extraordinarily high endemicity. Regional mountain isolation is probably the most effective driver for epiphyte diversification in Taiwan. Regarding the proportional contribution of epiphytic ferns and orchids, Taiwan is transitional between tropical and temperate zones. The disjunctive distribution of epiphytes between Taiwan and SW China as well as E Himalaya suggests low habitat similarity to adjacent China and/or a legacy of Late Quaternary climate change. Taiwanese vascular epiphyte distributions are in agreement with the Neo-Wallace Line.

Chapter 3 Regional and altitudinal patterns in vascular epiphyte richness on an East Asian island

In Taiwan, active orogenesis has created an extensive mountain system with high vegetation heterogeneity, providing diverse habitats for epiphyte growth.

CHAPTER 3

Regional and altitudinal patterns in vascular epiphyte richness on an East Asian island

Rebecca C.-C. Hsu, Jan H.D. Wolf & Wil L.M. Tamis

Abstract

The distribution of species on mountains has been related to various predictor variables, especially temperature. Thermal specialization, which is presumed to be more pronounced on tropical mountains than on temperate mountains, accounts for the elevational pattern of species richness and varies between organisms and geographic areas. In this study, the elevational and regional distribution patterns of 331 epiphyte species in Taiwan were explored using 39,084 unique botanic collections, mostly from herbaria. Species richness showed a peak in elevation between 500 and 1500 m. This peak could not be explained by a null model, the mid-domain effect, suggesting that environmental variables accounted mostly for the distribution of species on the mountains. Next, species distributions were modelled (with 30 predictor variables) to assess epiphyte regional and altitudinal distribution patterns. The model results not only corroborated the position of the mid-elevation peak in richness, they also identified two mountain areas on the island with exceptionally high species richness. These areas of high epiphyte diversity coincide with areas of high rainfall in relation to the direction of the prevailing winds. Moreover, a subsequent exploratory ordination analysis showed a varied thermal preference between epiphyte subcategories (hemiepiphytes, dicotyledons, orchids and ferns). In contrast to predictions by the Rapoport Effect hypothesis, ordination analysis also showed that the degree of thermal specialization increased with elevation, suggesting that highland species may be especially vulnerable to global warming. Finally, the partial ordination analysis controlling for all other variables suggested that typhoons exert a significant influence on the distribution of epiphytes.

EPIPHYTE DISTRIBUTION PATTERN

Fig. 1 The geographical location of Taiwan and climatic zones in the island according to the Köppen‐ Trewartha climate system. Ar = tropical wet climate (coolest month > 18°C), south‐eastern peninsula (< 500 m); Aw = tropical savannah climate (winter dry > two dry months), southern lowlands (< 500 m); Cfa = wet subtropical climate (warmest month > 22°C, no distinct dry season), island‐wide (< 500 m); Cwa = wet subtropical ‐winter dry climate (warmest month > 22°C), south‐western inland hills (500–1000 m); GCfa = mountain climate (warmest month > 22°C, no distinct dry season), island‐wide (500–1500 m); GCfb = mountain climate (warmest month < 22°C, no distinct dry season), island‐wide (1500–3000m). The central range, with an altitude > 3000 m is unshaded.

CHAPTER 3

Introduction

The distribution of species on tropical mountains has received renewed interest since high- elevation thermal specialists in the tropics could be among the most imperiled species on earth due to global warming (Laurance et al., 2011). Compared with species in temperate areas, species in the tropics experience limited annual thermal variability and presumed resulting thermal specialization may explain the generally relatively low elevation-range of species on tropical mountains (Janzen 1967). The degree of thermal specialization is nevertheless not universal, varying among taxa, elevations and geographic locations. Hence, studies with various species and from different areas are required to attain a complete picture. Moreover, the assessment of thermal specialization is obscured because, in addition to thermal factors, hydrological, biotic and other unknown factors may determine the distribution of species on mountains (Bruijnzeel et al., 2010). Another arguably characteristic of species in tropical areas is that mountain species have less thermal specialization than lowland species as an extension of Rapoport’s latitudinal rule (Stevens 1992). Accordingly, on small continental islands such as Taiwan, overall thermal specialists are relatively rare, largely due to a paucity of upper-zone specialists (Laurance et al., 2011).

Species distribution patterns on mountains account for the variability in species richness with elevation. Many organisms show a peak in species richness at mid-elevation (Laurance et al., 2011), and this is also true for epiphytes (Wolf and Flamenco-S 2003, McCain 2004, Cardelus et al., 2006). In addition to environmental factors, such as temperature, rainfall and fogs, and historical factors (Gentry and Dodson 1987a, Küper et al., 2004), the mid- elevation peak in species richness has been explained solely by applying a distribution null model (i.e. the mid-domain effect). The mid-domain effect arises from geographic constraints on species range within a bounded domain (Colwell and Lees 2000). Within a landmass boundary (e.g. from coasts to mountain tops), the null model predicts a peak in species richness at mid-elevation, simply based on overlapping species’ ranges. For epiphytic bryophytes in Colombia, the mid-elevation maximum in species richness was indeed explained by a mid-domain effect (Wolf 1993, Ah-Peng et al., 2012). In contrast, the richness of ferns on mountains was best accounted for by climatic factors (Kessler et al., 2011).

Here, we present for the first time data on the elevational distribution of epiphytes in Taiwan, an island in the western Pacific on the transition from tropical to subtropical latitudes. In Taiwan, active orogenesis has created an extensive mountain system with diverse vegetation types, ranging from alpine tundra to tropical rainforests. With approximately 4000 species of vascular plants (including ca. 600 Pteridophytes), the floristic diversity of Taiwan is exceptionally high compared with other (sub-) tropical islands (Dawson 1963, Reyes-Betancort et al., 2008, Creese et al., 2011). Taiwan is also one of the botanically best explored regions in

EPIPHYTE DISTRIBUTION PATTERN

Southeast Asia, and digitized herbarium collections contain over 200,000 records. Despite having immense plant diversity, Taiwan may be considered relatively poor in epiphytes. There have been ca. 350 species of vascular epiphytes reported for Taiwan, comprising only eight percent of the total vascular flora (Hsu and Wolf 2009), which is less than the worldwide level of 10 percent (Benzing 1990). In some wet tropical ecosystems, the native vascular flora may consist of up to 35 percent epiphytic species (Gentry and Dodson 1987a). Epiphytes are also poorly represented on tropical islands of the Caribbean, which has been attributed to geographical isolation and large-scale disturbances by tropical cyclones (Migenis and Ackerman 1993). In south Florida, a single cyclone (hurricane) may reduce the population density of epiphytic bromeliads by 12–43 percent (Oberbauer et al., 1996). Tropical cyclones (called typhoon in Asia) may also have a dramatic influence on forest canopies, increasing understorey light levels to 30 percent of outside levels (Lin et al., 2003).

The aim of this study was to assess patterns in the distribution of Taiwanese vascular epiphytes. In particular, we tested the following hypotheses: (1) epiphytes show a mid-elevation peak in species richness, (2) the peak in richness is explained by a mid-domain effect, (3) environmental forcing accounts for areas with high species richness, (4) hemiepiphytes, orchids, ferns and epiphytic dicotyledons have a different thermal preference on the mountain, (5) upper-zone thermal specialists are relatively rare in comparison with those in the lower zone, and (6) typhoons influence the distribution of epiphytes.

Methods

Study site

Taiwan is a 36,000 km2 tropical-subtropical transition island (21°45'–25°56'N and 119°18'E– 124°34'E). About 70 percent of the island is covered by mountains (> 1,000 m above sea level [asl]; Fig. 1), including more than 50 peaks > 3000 m in altitude. Annual rainfall ranges from 1000 mm to > 6000 mm, and falls mainly during the north-east (NE) monsoon (October– January) and during typhoon-induced heavy rain events (July–September). The NE monsoon accounts for 45 percent of the total annual rainfall in north-eastern Taiwan (Kao et al., 2004). On average, 3.7 typhoons hit Taiwan every summer (July–September), of which about 80 percent land on the east coast and track westbound (Wu and Kuo 1999). The torrential precipitation associated with typhoons mainly causes catastrophic damage to human lives and natural habitats. For example, the medium (category-2) typhoon Morakot (2009) brought 2777 mm rainfall in 72 h, triggering disastrous flooding, debris flows and landslides, especially in the mountain area. The typhoon induced-heavy rain supplied by south-westerly monsoon flows usually interact with the South China Sea summer monsoon (Xie and Zhang 2012). In addition, the dominated central range on the island often has complex interaction with the typhoon

CHAPTER 3 circulation, altering its structure, intensity and path, producing significant mesoscale variations in pressure, wind and precipitation distribution over Taiwan (Wang 1980). The central range may decrease the intensity of typhoons by an average of > 40 percent within 12 h of the storm centre reaching the island (Wu and Kuo 1999), thus typhoon impact is reduced in the western part of the island on the lee side of the central range.

Table 1. Predictors that were used for modelling species distribution, including four temperature‐ related (1–4), 12 precipitation‐related (5–16), nine topographic variables (17–25), and five land‐ cover/vegetation indices (16–30).

Predictor Description Unit 1 Tmean* Annual mean temperature 2 TcoldM Mean temperature of coldest month °C 3 TdryQ Mean temperature of driest quarter 4 Tsd* The standard deviation of the monthly mean No dimension temperatures 5 Pannual* Annual precipitation 6 PdryM Precipitation of driest month 7 PdryQ Precipitation of driest quarter Millimetre 8 PcoldQ Precipitation of coldest quarter 9‐14 P. 1, P. 4, P. 5, P. 6 P.7*, P.10* Monthly rainfall: January, April, May, June, July, October 15 Pdef Water deficiency: monthly precipitation minus Millimetre doubled monthly mean temperature minus °C 16 Pcv* The coefficient of variation of the monthly mean No dimension precipitation 17‐18 Eastness* Northness* Aspect transformed by sin(aspect rad) and Ordinal: 0–8 cos(aspect rad) 19 Soilcode Soil category Cardinal: 0–9 20 SoilPH Soil alkalinity Ordinal: 0–9 21 Estd The standard deviation of elevation within 1‐km2 No dimension 22 Elevation Altitude above sea level 23 Dto3000* The distance to the nearest location above 3000 m [asl] Metre 24 DtoSea The distance to the nearest coast 25 DtoRiver The distance to the nearest river 26 Landcover* Land‐cover classification Cardinal: 0–27 27‐30 EVI.1–4 Monthly enhanced vegetation index, EVI.1: spring (April to May), EVI.2: summer (June to September), EVI.3: NE monsoon initiation No dimension (October to November), EVI.4: slow growth season (December to March) * Predictors only used in model building for species with < 80 occurrences.

EPIPHYTE DISTRIBUTION PATTERN

Data collection

We compiled occurrences of epiphytic species in herbarium records, published plant inventories and our own botanical observations as a georeferenced epiphyte database that finally comprised 39,084 records in 331 species (24 families, 105 genera). Pteridophytes contributed most species (171), followed by orchids (120). The epiphyte species in the database were divided into four subcategories based on life form and taxonomy: hemiepiphytes, (abbreviation Hemis, e.g. Moraceae, Araceae), ferns and fern allies (Ferns), orchids (Orchids) and dicotyledons (abbreviation Dicots). For more detailed information on the species in the database, see Hsu and Wolf (2009).

To assess species richness patterns along the altitudinal gradient (Hypotheses 1 and 2), we used the entire epiphyte collection database. We computed species accumulation curves (sample-based rarefaction) and associated richness estimators (Chao 2005), using the freeware program EstimateS 8.2 (Colwell 2011). The species range midpoints were tested against the mid-domain effect hypothesis using Mid-Domain Null, a Monte Carlo based simulation programme, applying 1000 permutations without replacement (McCain 2004).

To evaluate regional species richness, species thermal niches and the influence of typhoons (Hypotheses 3 to 6), we subsequently assembled the plotless herbarium collection localities as records in grid cells with a spatial resolution of 1 km2. Multiple occurrences of the same species in a single cell were considered a ‘unique’ record. The final database comprised 28,693 records. A total of 252 species occurred in more than 10 cells, and the most widespread species occurred in 1613 cells. It is well known that systematic botanists have a bias for certain accessible localities and taxonomic groups, and the absence of species in cells is possibly due to insufficient sampling. To endeavour to fill in the distribution gaps, we used species distribution models (SDMs).

Epiphyte species distribution models

In our SDM, we used a maximum entropy method, MaxEnt (version 3.3.3k) (Phillips et al., 2006). In MaxEnt, species’ occurrences are related by predictor variables across a series of observation sites to recognize the realized niche of each species (Guisan and Thuiller 2005). Statistically speaking, the MaxEnt model minimizes the relative entropy between probability densities of species presence data and the background landscape (Elith et al., 2011). MaxEnt uses species presence-data only and we entered all species in the model that occurred in at least ten 1-km2 grid cells. Since MaxEnt puts no weight on the absence of a species, it is particularly suited for high-canopy epiphytes, which are often difficult to detect from the ground (Flores- Palacios and García-Franco 2001).

CHAPTER 3

Based on the ecological understanding of epiphytes, 30 environmental variables (Table 1) were selected for building SDMs at a resolution of 1-km2, comprising 35,928 grid cells in total. The predictors included nine topographic variables, 16 climatic (12 precipitation- related and four temperature-related) variables and five land-cover/vegetation indices. The land-cover classification (27 categories) was derived from data of a national vegetation inventory and mapping programme (Chiou et al., 2009) combined with satellite data from a global land cover facility (Hansen et al., 1998). An enhanced vegetation index (EVI) with improved sensitivity in high biomass regions was obtained from NASA’s Land Processes Distributed Active Archive Center (see URL http://reverb.echo.nasa.gov/reverb, averages from year 2001 to 2010). The monthly EVI was further summarized and averaged to represent annual patterns for spring (April–May), summer (June–September), NE monsoon initiation (October–November) and slow growing season (December–March). There was a degree of correlation among some of our predictors, such as mean temperature of coldest month and annual mean temperature. However, visual maps of these factors indicated regional heterogeneity in spatial patterns, despite a general similarity throughout most of the island. Certain small regions may provide ‘unique’ environmental requirements for species with restricted distribution. There is a reduced need for our modelling method MaxEnt to pre-select predictors, since it is more stable than most methods when dealing with correlated variables (Elith et al., 2011). In order to extract all possible information on regional spatial patterns, we used all thirty candidate predictors to build our SDMs, unless species were represented by only a few samples (< 80 records). For these rarer species, we pre-selected the candidate predictors to avoid over-parameterizing models using correlation tests and the result of a preliminary run of the model. Ten variables (Table 1) were indentified for modelling the distribution of species with less than 80 samples. To avoid misinterpretation and ensure model reliability, we also excluded species with fewer than ten records (79 species, 24%) from the SDMs. For different sample sizes (numbers of records), we used different model validation approaches and varied the MaxEnt settings for background samples and selection of features.

Background samples

In MaxEnt, a finite collection of points with associated covariates (environmental predictors) from the geographic area (landscape) of interest is called a background sample (VanDerWal et al., 2009). Conceptually, the landscape used for the background sample should include the full environmental range required by the species, and exclude the areas where species are unlikely to disperse. Areas that have not been surveyed because there is no suitable habitat for the species should also be excluded (Elith et al., 2011). In this study, we used the MaxEnt program’s default setting, randomly sampled 10,000 background locations from the given 35,928 grids of covariates covering the island for the common species (≥ 80 occurrences). We restricted backgrounds sampled from preferred epiphyte habitats for species with few records

EPIPHYTE DISTRIBUTION PATTERN

(< 80 occurrences) by deriving a set of 5000 backgrounds randomly sampled from the full set of epiphyte occurrences (29,087).

Features selection

MaxEnt uses the term ‘feature’to describe the transformation of predictors. Currently, MaxEnt has six feature classes: linear, product, quadratic, hinge, threshold and categorical. The programme by default (i.e. using Auto features) restricts models to simple features if few samples were introduced. When there are at least 80 training samples, all six feature types are used; features are excluded as sample numbers decline (for example, for 15–79 samples, the product and threshold features are excluded; for 10–14 samples, the hinge feature is excluded; and for < 10 samples, only linear features are used). We ran preliminary models using 10-fold cross-validation to estimate predictive performance via held-out data (Phillips 2008). For species with ≥ 80 samples, the test statistic (the area under the receiver operating characteristic curve [AUC]) was significantly higher when using all features than when using only the hinge feature as suggested by Elith et al., (2011). However, for species with few (< 80) samples, using auto features provided a significantly lower 10-fold cross-validated AUC than the linear and hinge features (the last two features had statistically equal AUC values). Nevertheless, the hinge feature exhibited many more violations of AIC (Akaike’s Information Criterion) values than the linear feature for species with few samples. Therefore, the final models were fitted on the full data sets (i.e. all samples for model training) using all feature types for species with ≥ 80 samples and using the linear feature for species with < 80 samples.

Model validation

We used several measures to validate the resulting SDMs. We calculated AIC values using ENMtools 1.3 to determine whether the models had more parameters than samples, which would have violated the assumptions of AIC (Warren and Seifert 2010). Three SDMs (containing < 80 samples) were excluded from later analyses at this stage. Next, we used a null method to test the model significance (Raes and ter Steege 2007). Models with the same settings as described above were fitted on 29 sets (each with a thousand permutations) of randomly chosen samples (with intervals of one for 5–30 records, intervals of five for 35–55 records, and intervals of ten for 60–80 records). We applied a curve-fit through the upper limit of the 95% confidence interval (CI) on the MaxEnt generated AUC values (1000 values per set) to identify which SDMs had a significantly higher AUC value than expected by chance alone (p < 0.05). There were 94 SDMs (< 80 samples) excluded from later analyses at this stage. We did not apply the null test to species with ≥ 80 samples because it had been found previously that models based on more than 80 samples were rarely insignificant (Hsu et al., 2012).

CHAPTER 3

Creating an epiphyte richness map (Hypothesis 3)

We obtained 156 validated SDMs, comprising 68 relatively rare (< 80 samples) and 88 common (≥ 80 samples) species. To create an epiphyte richness map, we applied a threshold of sensitivity-specificity sum maximization (Liu et al., 2005) to convert the MaxEnt probability distribution to a predicted presence map for each species. We then overlaid every single- species map to produce a species richness map for epiphytes in Taiwan.

Ordination analysis (Hypothesis 4-6)

We used a direct gradient ordination analysis, canonical correspondence analysis (CCA) to assess the thermal specialization of species and species groups and the influence of typhoons (Braak and Smilauer 2002). For predictor variables, we used the same 30 environmental variables that we used in MaxEnt (Table 1). For species, we used the same presence-absence data from the 156 epiphyte SDMs that we used to create the species richness map. To avoid multicollinearity, we performed a principal component analysis (PCA) on all variables. The first extracted PCA component was highly correlated with temperature: Tmean (Loading [L]: –0.27), TcoldM (L: –0.26), TwarmM (L: –0.26), TdryQ (L: –0.27) and Elevation (L: 0.26). The second PCA component was highly correlated with rainfall: Pcv (L: –0.30), PdryM (L: 0.29), PdryQ (L: 0.28), PcoldQ (L: 0.29), P01 (L: 0.29), PTY (L: –0.27), and P06 (L: –0.26). The first and second component together explained 52 percent of the variation. Both components were retained in the CCA, as opposed to a third component that had little additional explanatory value (9%). Next, the species and environmental variables (PCA component-1 and -2) were subjected to CCA We tested the significance of the first extracted CCA axis using a Monte Carlo test (999 permutations). CCA not only generates the species scores on the axes, but also their standard deviations (called tolerances in CCA), which may be seen as a measure of niche width (Lepš and Smilauer 2003). Hence, on a generated axis that is highly correlated with elevation, the species tolerance is a measure of thermal specialization.

We defined typhoon disturbance as the frequency of historical typhoons on the same 1 × 1 km grid (35,928 cells) as the other environmental predictors. Recorded traces and eyes of typhoons from 1958 to 2006 were plotted as circles with radii of Beaufort scale 7 and 10 (wind speed = 17.1 and 28.3 m/sec, respectively), and the accumulated numbers of typhoons per cell were calculated (Lin et al., 2006). To establish whether typhoon influenced the distribution of epiphytes, we performed a separate CCA analysis using our typhoon frequency data and 156 epiphyte SDMs, entering the PCA components of our 30 environmental predictors as covariables. Due to the complex interaction between the central range and typhoon circulation, which causes unpredictable changes in typhoon structure on the lee side of the central range, we excluded cells from the western part of the island. Therefore, we only considered cells east of the central ridge (10,725 grids) and past typhoons landing on the east coast of Taiwan to

EPIPHYTE DISTRIBUTION PATTERN explore the influence of typhoons on epiphyte vegetation. The ordination analyses were performed in R with vegan, a community ecology package (Oksanen et al., 2012, R Core Team 2012).

Results

Epiphyte species richness showed a peak in species richness between 500 and 1500 m (Table 2; Fig. 2). Although the difference between the species richness at < 500 m and richness at 500– 1000 m was small, it was significant (M = 306.03, SD = 8.53 and M = 308.33, SD = 9.47, respectively; paired t(24740) = 20.1, p < 0.05). Species richness showed a more rapid decrease above 1500 m. The elevation-species richness curve fell outside the 95% CI curves of the mid- domain null model curve (Fig. 3); hence the mid-elevation peak in richness could not be explained by a mid-domain effect.

Fig. 2 Epiphyte species accumulation curves based on sample‐based rarefaction (software program EstimateS 7). Collections per altitudinal interval: 12,944 (< 500 m), 11,798 (500–1000 m), 7,198 (1000–1500 m), 4,024 (1500–2000 m), 2,197 (2000–2500 m) and 923 (> 2500 m).

CHAPTER 3

Table 2. Number of epiphyte species per altitudinal interval in Taiwan; n = number of records, Sobs = the number of observed species, singletons = number of species that were only recorded once and Schao = estimated number of species for 95% CI and standard deviations (SD).

Altitudinal n S Singletons S S 95% CI SD interval obs chao chao < 500m 12944 286 39 306.03 (294.99, 330.59) 8.53 500–1000m 11798 289 29 308.33 (296.79, 336.98) 9.47 1000–1500m 7198 281 28 293.6 (285.91, 313.32) 6.42 1500–2000m 4024 235 39 276.17 (253.47, 326.76) 17.56 2000–2500m 2197 205 39 232.44 (217.43, 265.590 11.56 > 2500m 923 165 37 185.81 (174.2, 212.08) 9.06

Fig. 3 The species richness curve (with data points), based on 39,084 collections and 331 epiphytic species, and the 95% CI null model prediction curves sampled without replacement (software program Mid‐Domain Null, 1000 simulations).

EPIPHYTE DISTRIBUTION PATTERN

The mid-elevation peak in species richness was also shown by the epiphyte SDMs: most epiphyte species being found in the mild mountain climate of the GCfa Köppen- Trewartha climate zone between 500 and 1500 m (Fig. 1). The SDMs also identified two regions with high diversity on the western slope of the central range at mid-elevations: HsuehShan in northern Taiwan and AliShan in central Taiwan (Fig. 4A). Both areas are sheltered from east-coast landing typhoons and receive high amounts of annual rainfall under the influence of NE monsoons and SW flows, respectively. SDMs also showed considerable variation in distribution patterns between epiphyte subcategories. The most south-eastern tip of Taiwan (Fig. 1, HenChun peninsula) is characterized by a tropical wet lowland climate (Ar), and contained the highest percentage (11%) of hemiepiphytes (Hemis) of all the climatic zones. Epiphytic ferns were most often found in the cool mountain climate of the Köppen-Trewartha GCfb climate zone (67%), at an altitude of 1500–2500 m.

Fig. 4 (A) Modelled richness of pooled epiphytes (156 spp.) and two regions with exceptional high epiphyte diversity, namely HsuehShan and AliShan, both located at mid‐elevation (800–2000 m asl). (B) Richness pattern for the half of the modelled species (78 spp.) that had lower thermal tolerance values (i.e. the species with the highest thermal specialization). (C) Richness pattern for the other half of the modelled species that possessed higher thermal tolerance values.

CHAPTER 3

The thermal preference of the subcategories was also indicated by the CCA analysis. The distribution of the species on a significant first axis (explained variance 15.0%, Monte Carlo, p = 0.001) constrained by elevation, PCA component-1, indicated that hemiepiphytes (e.g. Ficus spp.) were predominately found at lower elevations, whilst epiphytic ferns (e.g. Crypsinus quasidivaricatus, Lepisorus clathratus and L. suboligolepidus) were the most prominent low temperature specialists (Fig. 5). Epiphytic orchids were found from low elevations (e.g. Liparis grossa and Appendicula reflexa) to upper mountains (Gastrochilus hoii). The thermal specialization (inverse niche-width) of the 156 analysed species was higher with increasing elevation, particularly for some epiphytic ferns and orchids (Pearson´s R = -0.39, p < 0.001, Fig. 6). Moreover, the half of the species (78 species) possessing relatively high thermal specialization (low tolerance values) exhibited an obvious mid-elevational pattern (Fig. 4B) in comparison to the indistinct distribution of the other half of species with a higher tolerance value (Fig. 4C).

Fig. 5 CCA ordination diagram of the species scores (156 spp.) on the first two axes with epiphyte species arranged by subcategory: orchids (open squares), ferns (open triangles), hemiepiphytes (black diamonds) and dicotyledons (black circles). The first axis (eigenvalue 0.4534, explaining 15% of total variance; Monte Carlo p < 0.001), is highly correlated with temperature (elevation), with higher elevation shown towards the right. The second axis (eigenvalue 0.1173, explaining 4% of variance) is related to water availability, with reduced water availability shown towards the top.

EPIPHYTE DISTRIBUTION PATTERN

Fig. 6 Species scores (156 spp.) on the first constrained canonical axis generated by CCA and standard deviations. The first axis is highly correlated with temperature (elevation), and thus its standard deviation (i.e. tolerance) may be interpreted as a measure of niche‐width. The thermal tolerance of the species is lower (i.e. higher thermal specialization) with increasing elevation towards the right (Pearson´s R = –0.39, p < 0.001). Epiphyte species are arranged by subcategory: orchids (open squares), ferns (open triangles), hemiepiphytes (black diamonds), and dicotyledons (black circles).

Independent of thermal and rainfall influences (PCA component-1 and component- 2), partial CCA showed that typhoons also exert an influence on the distribution of epiphytes (explained variance 1.6%, Monte Carlo p < 0.001; Fig.7). The two typhoon intensities that we analysed (scales 7 and 10) had largely opposing effects on the epiphyte community.

Discussion

In agreement with many tropical epiphyte studies from the American continent (Gentry and Dodson 1987a, Wolf 1993, Wolf and Flamenco-S. 2003, Krömer et al., 2005, but see Ibisch et al., 1996), our analyses, which used both empirical collections and SDMs, showed that vascular epiphytes had a peak in species richness at a mid-elevation on mountains. Recognizing that botanic collections are essentially non-random, we nevertheless presume that, for our data, a meaningful assessment of the observed distribution and diversity patterns is possible because of the extremely high number of unique records in the database (39,084).

CHAPTER 3

Fig. 7 Partial CCA ordination diagram with typhoon scales (arrows) as variables and epiphyte species arranged by subcategory: orchids (open squares), ferns (open triangles), hemiepiphytes (black diamonds) and dicotylendons (black circles). Independent of temperature and water availability, typhoons exert a significant influence on epiphyte distributions (explaining 1.6% of variance; Monte Carlo p < 0.001).

The mid-elevational peak in species richness could not explained by a null model. The result indicated a substantially higher species richness, and a richness peak at slightly lower elevations than expected by the null test. A similar pattern has also been described for an Indian Ocean island (Ah-Peng et al., 2012). Such a pattern is probably explained by the Massenerhebung effect (i.e. mountain mass elevation effect; Schroeter 1908, Bruijnzeel et al., 1993). This phenomenon occurs on isolated, small coastal mountains, where floristically-similar vegetation types tend to distribute at lower altitudes than on large mountain masses due to climatic compression. Moreover, the exceptionally high species richness observed at island mid-elevation may be augmented by a large number of species with a small range size in relation to fine niche partitioning. For instance, the restricted altitudinal band of Chamaecyparis- dominated cloud forest (1800–2500 m), characterized by low temperatures and continuously moist and dim conditions, is inhabited by no less than 92 species of rare ferns (Moore 2000). Environmental factors may thus account for the observed epiphyte distribution and, with this in mind, our approach using SDMs to complement grid cells with absent species is not unreasonable.

The SDMs identified two centres of epiphyte diversity, one in the north (HsuehShan) and another in central Taiwan (AliShan). Both areas are at a mid-elevation (800–2500 m asl)

EPIPHYTE DISTRIBUTION PATTERN and are also subject to significant precipitation, being under the influence of the NE monsoon in the winter or the SW rains that follow typhoons in the summer, respectively. Prevailing winds probably import diaspores to these two regions, since the majority of epiphytes in Taiwan (89%) are wind dispersed (Hsu and Wolf 2009); the ferns Asplenium hondoense and A. pekinense, which have an affinity with temperate East Asia and Japan, are only found in small regions under the influence of the NE monsoon (Moore 2000). Humid conditions and accessibility probably both contribute to the presence of areas of high epiphyte richness and endemism. Accordingly, the HsuehShan and AliShan regions merit special attention from conservationists.

The SDMs also showed that whilst epiphytic ferns were relatively common in northern Taiwan, central Taiwan has a relatively high number of epiphytic orchids. Central Taiwan receives little influence from the NE monsoon and is therefore relatively dry and warm in winter. Thus, in agreement with many other epiphyte studies (Gentry and Dodson 1987a, Benzing 1990, Wolf 1994), the SDMs confirmed that, of all environmental predictors that were used in the models, elevation and water availability accounted to great extent for the distribution of epiphytes in Taiwan.

The relative importance of temperature (elevation) and water availability was also demostrated by the exploratory multivariate ordination analysis, where temperature was identified as the most important variable. In agreement with patterns in the neotropics (Wolf and Flamenco-S. 2003, Benavides et al., 2010), hemiepiphytes such as aroids and Ficus species dominated moist stream valleys in the lowlands (< 1000 m asl), especially in the south-eastern peninsula where monthly mean temperature was > 18 ˚C. As in the Andes, epiphytic ferns were particularly adapted to mountain climates (Kessler 2011); the epiphytic fern Crypsinus quasidivaricatus (Hayata) Copel was recorded near the timberline (3500 m asl).

Interestingly, our results showed that thermal specialization or inverse thermal niche- width was not uniform along the elevational gradient, but increased with altitudes. Epiphytic ferns in Bolivia show a similar pattern (Kessler 2011). However, this pattern contrasts with the Rapoport effect hypothesis, which suggests that the elevational ranges of species are greatest at higher altitudes, and consequently thermal-specialist species are more likely to colonize lower altitudes than higher altitudes (Stevens 1992, Laurance et al., 2011). Studies on thermal specialization in tropical mountains are clearly not conclusive. Our study identified several montane cloud forests at mid-elevations with many epiphytic thermal specialists. In mid- elevational cloud forests, the frequently occurring fog events lead to little diurnal (and seasonal) thermal variation, which according to the Rapoport effect promotes thermal specialization and susceptibility to global climate change (Foster 2001, Mulligan 2010, Ah-Peng et al., 2012).

CHAPTER 3

The ordination analysis also suggested for the first time that typhoons have a significant influence on the distribution of epiphytes, independent of the temperature- and humidity-related variables that were used in our analysis. Typhoons may directly blow epiphytes of their hosts, or indirectly alter the microclimate through mechanical defoliation of canopies (Mabry et al., 1998). Hemiepiphytes, such as strangler figs and aroids, seem relatively resistant to direct wind-blow in terms of their tightly-attached adventitious roots on hosts, which may explain why they are largely found on the south-eastern peninsula of Taiwan, despite ca. 11 percent of all typhoons landing in this region. Whereas powerful typhoons can be damaging to epiphytes, moderate typhoons are likely less damaging or may even promote epiphyte proliferation because of the significant accompanying precipitation. This may explain why Beaufort scale 10 and scale 7 typhoons have differing effects on epiphyte distributions. Further field studies are necessary to properly identify how typhoon may affect epiphyte distribution, which currently remains elusive.

Chapter 4

Canopy CO2 concentrations and crassulacean acid metabolism in Hoya carnosa in a subtropical rain

forest in Taiwan: consideration of CO2 availability and the evolution of CAM in epiphytes

Fushan is a subtropical rainforest with annual rainfall above 3.5 m. Although here the average daily humidity throughout the year typically approaches 95 %, our study indicated that the likely ecophysiological significance of CAM Hoya carnosa in H. carnosa remains water conservation rather than CO2 availability. CHAPTER 4

Canopy CO2 concentrations and Crassulacean acid metabolism in Hoya carnosa in a subtropical rain

forest in Taiwan: consideration of CO2 availability and the evolution of CAM in epiphytes

R. C.-C. Hsu, T.-C. Lin, W.-l. Chiou, S.-H. Lin, K.-C. Lin & C. E. Martin

Photosynthetica 44, no. 1 (2006): 130-135

Abstract

The potential importance of CO2 derived from host tree respiration at night as a substrate for nighttime CO2 uptake during CAM was investigated in the subtropical and tropical epiphytic vine Hoya carnosa in a subtropical rainforest in northeastern Taiwan. Individuals were examined within the canopies of host trees in open, exposed situations, as well as in dense forests. Although nighttime CO2 concentrations were higher near the epiphytic vines at night, relative to those measured during the day, presumably the result of CO2 added to the canopy air by the host tree, no evidence for substantial use of this CO2 was found. In particular, stable carbon isotope ratios of H. carnosa were not substantially lower than those of many other CAM plants, as would be expected if host-respired CO2 were an important source of CO2 for these CAM epiphytes. Furthermore, laboratory measurements of diel CO2 exchange revealed a substantial contribution of daytime CO2 uptake in these vines, which should also result in lower carbon isotope values than those characteristic of a CAM plant lacking daytime CO2 uptake. Overall, the results of this study indicate that host-respired CO2 does not contribute substantially to the carbon budget of this epiphytic CAM plant. This finding does not support the hypothesis that CAM may have evolved in tropical epiphytes in response to diel changes in the CO2 concentrations within the host tree canopy.

Introduction

Of the three major photosynthetic pathways found among plants, Crassulacean acid metabolism (CAM) is unique in that atmospheric CO2 is absorbed primarily at night via open stomata (Kluge and Ting 1978, Osmond 1978, Winter 1985, Lüttge 1987). As a result of PEP carboxylase activity, the absorbed CO2 is converted to oxaloacetate, which is then reduced to malate. Throughout the night, the malate is stored in the vacuoles as malic acid. During the

CAM EVOLUTION IN EPIPHYTES day, the malic acid leaves the vacuoles and is decarboxylated. The resultant accumulation of

CO2 effects daytime stomatal closure while the CO2 is slowly reduced to carbohydrate via the typical C3 photosynthetic machinery. By opening their stomata at night and closing them during the hotter and drier day, CAM plants lose considerably less water during photosynthesis, i.e., have much higher water-use efficiencies (WUE), relative to C3 and C4 plants (Kluge and Ting 1978, Osmond 1978, Winter 1985, Lüttge 1987). Therefore, it is not surprising that many CAM plants grow in arid regions of the world. In addition, even more CAM taxa, primarily in the form of epiphytes, are found in tropical and subtropical areas (Winter 1985, Lüttge 1989, Winter and Smith 1996). This too is not surprising, given that drought stress is frequently endured by epiphytic plants between periods of precipitation (Winter 1985, Lüttge 1989, Benzing 1990, Martin 1994).

In the past decade, CAM has also been reported among various taxa of submerged aquatic plants (Keeley 1996). Clearly, minimization of water loss (high WUE) was not a selective force in the evolution of CAM in such plants. Instead, several studies have shown that low daytime CO2 availability, coupled with high nighttime availability, constitutes an important benefit of CAM in these aquatic plants (Keeley 1996).

As indicated above, the widespread occurrence of CAM among epiphytes is not surprising as a result of short, but potentially frequent periods of drought stress. On the other hand, reports of CAM in epiphytes that are found in the understory and/or dense canopies of rain forests in tropical and subtropical regions with extremely abundant and frequent rainfall and a short or no dry season are puzzling (e.g., Martin et al., 1981, 1985, Winter et al., 1983, 1986, Adams 1988, Adams et al., 1988, Griffiths 1988, Kluge et al., 1989, Carter and Martin

1994, Skillman and Winter 1997, Martin et al., 2005). Because atmospheric CO2 concentrations in the C3 host canopies are higher at night due to respiration of the canopy leaves, relative to the canopy atmosphere during the day when the host leaves are absorbing CO2 (see references below), it is tempting to speculate that, as in aquatic CAM plants, CAM might have evolved in such epiphytes in response to CO2 availability instead of drought stress (Knauft and Arditti 1969, Benzing 1990, Carter and Martin 1994). With this speculation in mind, the goal of the present study was to determine the degree to which an epiphytic CAM plant utilizes CO2 respired by its host tree at night. Although evidence that extensive usage of such CO2 might be construed as lending support to the hypothesis that CAM evolved in such plants in response to CO2 availability, evidence to the contrary would be difficult to reconcile with this hypothesis.

CHAPTER 4

Materials and methods

Study area and plants

The study site was located in a semi-disturbed area (allowing greater accessibility to the plants) in the Fushan Experimental Forest, a subtropical rain forest at 600 m elevation, in northeastern Taiwan (longitude 121°34’ E, latitude 24°26’N). Species of dominant trees at this site were numerous and were primarily in the families Fagaceae and Lauraceae. Climatic conditions at Fushan are subtropical, with monthly average air temperatures ranging from 10 to 25 °C and monthly rainfall ranging from less than 10 cm to 50 cm, with maxima occurring in the summer months (annual rainfall is 3.56 m). Even in January, the month with the lowest average rainfall, humidities are very high, and rain falls on an average of 20 days of the month; thus, there is no true dry season at Fushan. The average daily humidity throughout the year typically approaches 95 %.

In mid-June 2001, twenty Hoya carnosa plants were selected, ten in trees growing in intact, dense stands of forest (referred to here as “closed” canopies) and ten in trees in the open with few neighbors (“open” canopies). The latter trees were often in clearings or near sparsely used roads. Canopy openness and penetration of direct and diffuse irradiance into the canopy were measured with a Nikon 4500 digital camera, Nikon FC-E8 fisheye lens, and the software program Delta-T Hemiview Canopy Analysis Software (Cambridge, UK; Lin et al., 2003). Photographs were taken at a height of two meters in the canopy of each tree by holding the camera adjacent and perpendicular to H. carnosa individuals and recording exposures in three directions outward from the tree trunk. These three measurements were then averaged for each tree. In all cases, individuals of H. carnosa were epiphytic vines extending vertically along most of the tree trunks.

Atmospheric CO2 concentrations

Air CO2 concentrations at mid-day (11:00 – 13:00 hours) and mid-night (00:00 – 03:00 hours) were measured using a LI-COR (Lincoln, NE) LI-6400 Portable Photosynthesis System at a height of two meters, the same height at which leaves were sampled for acidity and carbon isotope ratios. Air was sampled within 10-20 cm of the H. carnosa plants. No rain fell during the night and day of measurements; the day during which air was sampled was partly sunny and warm. The air was calm during both sets of measurements.

Leaf titratable acidity

Shortly before sunset and again shortly after sunrise, a leaf was removed from each of the H. carnosa plants and frozen (-10 °C) within five minutes of excision. The days on which the

CAM EVOLUTION IN EPIPHYTES leaves were sampled were partly sunny and warm. After two days in the freezer, the leaf was thawed, and a portion was weighed and pulverized in distilled water in a mortar and pestle. The resultant slurry was titrated to pH 7.0 using 0.01 N NaOH. After titrating, the water was evaporated, and the dry mass of the tissue was obtained after a week in an oven at 70 °C.

Leaf carbon isotope ratios

Leaves of the H. carnosa individuals and of their host trees were collected and dried for at least a week at 70 °C, then ground into a powder and combusted for determination of the stable isotopic composition of their carbon at the University of Arkansas Stable Isotope Facility using a Carlo Erba elemental analyzer (NA1500 CHN Combustion Analyzer, Carlo Erba Strumentazione, Milan, Italy) coupled to a Finnigan Delta+ mass spectrometer (Finnigan MAT, Bremen, Germany) via a Finnigan Conflo II interface. The spectrometer had been calibrated using the PDB standard. The instrument error (twice the standard deviation) associated with each measurement was ± 0.1 ‰.

Shoot gas exchange

Plants were collected at the study site, transported to the University of Kansas, and grown in potted soil in a growth chamber under the following conditions: 50-100 μmol m-2 s-1 photosynthetic photon flux density (PPFD), 30/20 °C day/night air temperatures, 2.43/0.52 kPa day/night vapor pressure deficits, and a photo/thermoperiod of 12 hours. After three years of growth under these conditions, plants were large, vigorous, and flowering. Shoots with two to four leaves were sealed in gas exchange cuvettes, and net CO2 exchange was measured continuously for three days under environmental conditions similar to those in the growth chamber. The open gas exchange system comprised: a LI-COR LI-6262 differential infrared gas analyzer; polycarbonate, water-jacketed gas exchange cuvettes with small fans for air mixing; thermocouple and thermistor temperature sensors and meters for air and leaf temperature measurements; a temperature-controlled humidifier; and a computer for data collection. Further details of this system, as well as methods of data analysis, have been previously described (Harris and Martin 1991, Gravatt and Martin 1992).

Statistics

In most cases, pairs of means were compared using the Student’s t-test or the Mann-Whitney U-test whenever the data failed to meet the assumptions of the parametric t-test (Sokal and

Rohlf 1981). Day and night air CO2 concentrations measured in the closed and open canopies were compared with a two-way analysis of variance, followed by the Tukey comparison-of- means test (Sokal and Rohlf 1981). In all tests, statistical significance was inferred when P ≤ 0.05.

CHAPTER 4

Results and discussion

All individuals of H. carnosa performed CAM, as evidenced by significant and substantial accumulations of acidity in the leaves at night (Fig. 1; also see gas exchange findings below). Plants in the open canopies exhibited much higher acid accumulations, presumably a result of the increased availability of irradiance in the more exposed trees (see Fig. 2), although the latter conclusion is in direct contrast to the conclusions of past studies of sun/shade adaptations in three species of Hoya, including H. carnosa (Winter et al., 1983, Adams et al., 1987, 1988). On the other hand, some data from these studies support those of the current study; nocturnal acid accumulations for plants growing in the field in Australia were greater in plants growing in full sunlight, relative to values for plants growing in deep shade. Thus, it is clear that more work is required before the sun/shade status of epiphytic species of Hoya is fully understood.

2000 ] -1 1500 mol g  1000

500 Leaf acidity [ Leaf acidity

0 open closed

Fig. 1 Mean morning (black bars), evening (light gray bars), and overnight increases in (dark gray bars) acidity of leaves of Hoya carnosa in open and closed host tree canopies in a subtropical rain forest in northeastern Taiwan. The error bars are standard deviations (n = 10). Differences between both sets of morning/evening means and between the mean overnight increases in leaf acidities are highly significant (P < 0.001).

CAM EVOLUTION IN EPIPHYTES

0.5

0.4

0.3

0.2 canopy/open 0.1

0.0 openness direct diffuse

Fig. 2 Mean measures of irradiance penetration into the canopy of host trees at a height of two meters and adjacent to individuals of Hoya carnosa in a subtropical rain forest in northeastern Taiwan. The error bars are standard deviations (n = 10). Canopy openness is the fractional area of all gaps in the canopy; direct irradiance is the proportion of direct PPFD, relative to that in the open; and diffuse irradiance is the proportion of indirect (diffuse) PPFD, relative to that in the open. All values are based on photographic images and are relative to measurements taken in a fully exposed (open) location nearby. In all cases, the open canopies (black bars) allowed more irradiance (P < 0.001) to the H. carnosa vines than did the closed canopies (gray bars).

The CO2 concentration of the atmosphere in the host tree canopies in the Fushan rain forest was 40-60 μmol mol-1 higher at night than during the day, regardless of the closed or open nature of the forest canopy (Fig. 3). In addition, nocturnal CO2 concentrations were higher in the closed canopies (trees in dense forest), relative to the open canopies of the more exposed trees. This was not the case during the day (Fig. 3). The day/night changes in canopy

CO2 concentrations at a height of two meters in this Taiwanese subtropical rain forest are not unlike those found at this height in a temperate deciduous forest in Japan (Koike et al., 2001). Although the latter study reported somewhat larger day/night differences (around 100 μmol -1 mol ), CO2 concentrations were measured at dawn and dusk, as opposed to the mid-day and mid-night measurements in the current study. At another site in Taiwan (approximately 400 km southwest of Fushan), the air CO2 concentrations at a height of two meters in the forest ranged from diurnal minima around 345 μmol mol-1 to nocturnal maxima of approximately 390 μmol mol-1 (Cheng and Kuo 2004), a diel change of 45 μmol mol-1, which is in the range of values reported here for the forest at Fushan.

CHAPTER 4

As expected for a CAM plant, the stable carbon isotope ratios of the epiphytes were substantially less negative than those of the host trees (Fig. 4), reflecting, in large part, the discriminatory properties of Rubisco versus PEP carboxylase (Kluge and Ting 1978, Holtum et al., 1982, Winter 1985, Griffiths 1992, 1993). As was the case with the host trees, the stable carbon isotope ratios of the epiphytes found in the closed canopies were not significantly different from those of the epiphytes in the open canopies (Fig. 4). Values reported in the current study fall between those reported for H. nicholsoniae growing in “deep shade” in an Australian rain forest (-14.33 ‰; Winter et al., 1986) and those of H. carnosa growing at various PPFD levels in a glasshouse also in Australia (-20.1 to -22.2 ‰; Adams et al., 1987).

]

-1 480

440 mol mol 

400

360 concentration [ 2 320 Air CO

Open Closed

Fig. 3 Mean mid‐night (black bars) and mid‐day (gray bars) CO2 concentrations of the air in the canopies of host trees at a height of two meters and adjacent to individuals of Hoya carnosa in a subtropical rain forest in northeastern Taiwan. The error bars are standard deviations (n = 10). The differences in mean CO2 concentrations between hosts with open and closed canopies were significant (P < 0.05), as were differences between night and day (P < 0.001). In addition, the interaction between canopy closure and time of day was significant (P < 0.05).

CAM EVOLUTION IN EPIPHYTES

C [- per mil] C [- per 20 12 C/ 13  10 Leaf Leaf

0 host host Hoya Hoya (open) (closed) (open) (closed)

Fig. 4 Mean δ13C/12C values (‐ ‰) of leaves of Hoya carnosa (gray bars) and their host trees (black bars; open and closed canopies) in a subtropical rain forest in northeastern Taiwan. The error bars are standard deviations (n = 10). Differences between open and closed host canopies in both sets of plants were not significantly different (P > 0.05).

The general goal of this study was to provide evidence that might be used in support of or against the hypothesis that CAM might have evolved in tropical epiphytes in response to increased CO2 availability at night. Air CO2 concentrations within the host tree canopies were indeed substantially higher at night than during the day. Because the host trees were all C3 plants, this respired air would be highly depleted in 13C, and its stable carbon isotope value would be similar to that of the host leaves, i.e., around -30 ‰ (Rundel et al., 1989, Griffiths 1993). Thus, the air surrounding the epiphytes should have an isotopic composition that represents a mixture of air from above the canopy, presumably with a carbon isotope ratio around -8 ‰ (Rundel et al., 1989, Griffiths 1993), with the host-respired air. As a result, although the stable carbon isotope ratio of the canopy air was not measured, its value was presumably more negative, and probably substantially so, than -8 ‰. Indeed, several studies have reported more negative carbon isotope ratios of the air and plant tissues inside tropical forests as a result of respired CO2 (Medina and Minchin 1980, Schleser and Jayasekera 1985, Da Silveira et al., 1989, Medina et al., 1986, 1991). Therefore, the stable carbon isotope ratios of the H. carnosa plants were predicted to be substantially lower than values for most CAM plants, especially those growing in more exposed locations (for a study using a similar rationale

CHAPTER 4 and approach, see Treseder et al., 1995). Confirmation of this prediction would lend support to the feasibility of the hypothesis about the evolution of CAM in epiphytes stated above.

Despite this expectation, the stable carbon isotope ratios of the H. carnosa epiphytes (Fig. 4) were not substantially more negative than values typical of many terrestrial CAM plants that grow in exposed habitats with few neighbors, e.g., desert succulents (Troughton et al., 1974, Eickmeier and Bender 1976, Sutton et al., 1976, Ting 1989). In addition, laboratory measurements of gas exchange using plants of H. carnosa collected at the study site revealed substantial amounts of daytime CO2 uptake (Fig. 5), which would result in carbon isotope ratios more negative than those of CAM plants lacking daytime CO2 uptake (Winter and

Holtum 2002). Furthermore, although nighttime CO2 concentrations were higher in the closed canopies, the stable carbon isotope ratios of the epiphytes in these canopies were not more negative than the values for the epiphytes in the open canopies. These findings indicate that H. carnosa does not utilize CO2 respired by the host tree canopy, at least to a substantial degree, in spite of the elevated CO2 concentrations in the canopy at night relative to during the day. Although a different species, the relatively high (less negative) carbon isotope value reported for H. nicholsoniae in a dense forest canopy (see above; Winter et al., 1986) also indicates a minimal contribution of host-respired CO2 to the carbon budget of this epiphytic CAM plant.

It is surprising that host-respired CO2 does not contribute more to the carbon composition of these epiphytic CAM plants. Although the weather was calm, and canopy air turbulence was not observed during the measurements made in this study, it is possible that the canopy air is typically less stagnant than this, mixing frequently with the atmosphere above the forest canopy and thereby diluting the contribution of host-respired CO2 to the canopy air. Canopy air turbulence measurements throughout the year are needed in order to test this explanation.

The results of this study do not lend support to the hypothesis that CAM might have evolved in tropical/subtropical epiphytes in response to atmospheric CO2 availability. Of course, different results might be obtained with other species of epiphytic CAM plants in other forests. The potential for the utilization of substantial amounts of host-respired CO2 in tree canopies should be investigated in more epiphytic CAM plants before definitive conclusions are drawn. At least in the case of H. carnosa in this subtropical rain forest, the likely ecophysiological significance of CAM remains water conservation, which should prove beneficial to such plants despite the infrequent occurrence of drought in this rain forest.

CAM EVOLUTION IN EPIPHYTES ] -1 0.8 s -1

0.6

0.4

0.2 exchange [nmol g 2 0.0

Net CO 10 14 18 22 26 Time of day

Fig. 5 Net CO2 exchange for a shoot of an individual of Hoya carnosa collected in a subtropical rain forest in northeastern Taiwan, then grown and measured in Kansas. The thick, horizontal black line indicates the nighttime. Environmental conditions during measurements are provided in “Materials and methods.”

Chapter 5 Comparative photosynthetic capacity of abaxial and adaxial leaf sides as related to exposure in an epiphytic fern in a subtropical rainforest in northeastern Taiwan

The Asplenium bird’s nest fern often forms a conspicuous layer in the forest canopy. Among three species in Taiwan, A. antiquum is usually found coexisting with A. nidus. The two species are morphologically very similar, but can be distinguished by the width of the scales on their leaf bases.

A. nidus A. antiguum

CHAPTER 5

Comparative photosynthetic capacity of abaxial and adaxial leaf sides as related to exposure in an epiphytic fern in a subtropical rainforest in northeastern Taiwan

Craig E. Martin, Rebecca C.-C. Hsu & Teng-Chiu Lin

American Fern Journal 99, no. 3 (2009): 145-154

Abstract

Photosynthetic gas exchange was measured in situ with either the adaxial or abaxial leaf surface illuminated on vertical, horizontal, and angled leaves of Asplenium nidus, an epiphytic ferns in a subtropical rain forest in northeastern Taiwan. Leaves for gas exchange measurements were selected to ensure a diversity of different exposures of the two leaf surfaces to direct sunlight. For most leaves of Asplenium nidus, photosynthetic rates were higher when the side of the leaf that typically received more direct insolation was illuminated during the gas exchange measurement. Higher rates of net CO2 uptake when one side of the leaf was illuminated, relative to rates when the opposite side was illuminated, were attributable to a greater biochemical capacity for photosynthesis, not to greater stomatal conductances. Based on the results of this study, the photosynthetic capacity of the two sides of the leaves of epiphytic ferns, for the most part, reflects the degree of exposure of each side of the leaf to direct sunlight, as has been found in similar studies of terrestrial taxa.

PHOTOSYNTHETIC PLASTICITY IN EPIPHYTES

Introduction

Most leaves are green and, thus, presumably capable of some level of photosynthetic activity, even if just recycling respiratory CO2, on both their adaxial and abaxial surfaces (Moore et al., 1998; Terashima, 1986). Work with terrestrial taxa has shown that the capacity for photosynthesis is equal, or nearly so, when either leaf surface of vertically oriented leaves is illuminated, as long as both surfaces intercept similar amounts of solar radiation during leaf development (Syvertsen and Cunningham, 1979; DeLucia et al., 1991; Poulson and DeLucia, 1993). In contrast, if one side of a vertically oriented leaf typically receives more insolation than the opposite side, the photosynthetic capacity of the leaf is greater when the normally sunlit surface is irradiated during photosynthetic measurements, relative to photosynthesis when the shaded side is irradiated (Poulson and DeLucia, 1993; but see Václavík, 1984) Likewise, the photosynthetic activity of horizontally oriented leaves is greater when their adaxial surface is illuminated than when their abaxial surface is illuminated (Syvertson and Cunningham, 1979; Terashima, 1986; DeLucia et al., 1991) The latter applies only to the sun leaves, not the shade leaves, of Sitka spruce (Leverenz and Jarvis, 1979).

Epiphytic vascular plants appear to have been excluded from such studies, yet are ideal subjects for such investigations. Epiphytic vascular plants often exhibit a great diversity of leaf orientations and exposures (Benzing, 1990). For example, epiphytes with a rosette growth form often have leaves ranging from vertical to horizontal, and many have intermediate angles. Most epiphytes also live in a complex light environment, being shaded by the host tree stem and canopy, as well as surrounding trees, depending on the location of the sun at any point in time. Given their leaf angles and the complexity of the light environment in which epiphytes grow, it is difficult to predict how the photosynthetic capacity of the two sides of the leaves of such plants compare and whether or not findings based on terrestrial taxa might apply to epiphytes. Therefore, the goal of this study was to determine if photosynthesis in epiphytes, particularly ferns, responds to leaf surface illumination in a similar manner as has been found in terrestrial plants.

Materials and methods

Study site and species

Leaf photosynthetic parameters were measured for six individuals of Asplenium nidus L. in situ at the Fushan Experimental Forest, a comparatively pristine tract of subtropical rainforest (121°34′E, 24°46′N) at an elevation of ca. 600 m located 40 km southeast of Taipei in northeastern Taiwan. For general climatic conditions at the Fushan site, see Martin et al. (2004). Environmental conditions during the week of measurements (11-15 July 2005) were: 25.1° C

CHAPTER 5 average daily air temperature (29.8° C average daily maximum; 21.3° C average daily minimum), 4.2 mbar average daily vapor pressure deficit (vpd); and 20.0 mol m-2 day-1 average daily Photosynthetic Photon Flux Density (PPFD).

Asplenium nidus was chosen for this investigation to ensure a diversity of different exposures of the two leaf surfaces to direct sunlight. Plants were selected in a partially disturbed section of the forest to allow easy access for in situ measurements of photosynthesis. The study site included several walking trails and was tens of meters from a laboratory building. Species of dominant trees at this site were numerous, primarily in the families Fagaceae and Lauraceae; examples include Litsea acuminata (Bl.) Kurata (Lauraceae), Machilus zuihoensis Hayata (Lauraceae), Castanopsis cuspidata (Thunb. ex Murray) Schottky var. carlesii (Hemsl.) Yamazaki (Fagaceae) and Pasania hancei (Benth.) Schottky (Fagaceae).

All plants were large (plant diameter for A. nidus ≥ 0.5m) growing epiphytically on a variety of host trees, including those listed above. Most plants had sporangia on some leaves at the time of this study (sporangia-bearing portions of the leaves were avoided in all measurements to avoid effects of sporangia on the measurements (Chiou et al. 2004). All leaves were measured no higher than three to four meters from the ground, i.e., within arm’s reach while standing, with or without a ladder. Only mature, non-senescent leaves lacking substantial insect damage were sampled; very young and very old leaves were avoided. Leaves were selected without regard to host tree species, height from the ground (except as noted), and degree of canopy shade at the time of measurements.

Photosynthesis measurements

Photosynthesis was measured on three different leaves for each of six plants of A. nidus; the three leaves were selected for measurements based primarily on the likelihood of exposure of each leaf surface to direct sunlight. Horizontal leaves were older (based on size, presence of sporangia, weathering, and phyllotaxy of the epiphyte) than the other two leaves selected for measurements and grew perpendicular to and away from the host tree trunk. Such leaves should intercept very little direct sunlight on their abaxial surface, whereas their adaxial surface should intercept direct sunlight during much of a sunny day. Angled leaves grew at about a 45 degree angle from the tree trunk, so should occasionally intercept direct sunlight on both surfaces of the leaf. Vertical leaves grew close to the trunk of the host tree, and, thus, were shaded by the trunk much of the day. These leaves should intercept little light on their outward-facing adaxial surface most of the day, but occasionally direct sunlight on their abaxial surface, depending on the location of the sun.

Photosynthesis was measured with a LI-COR (Lincoln, NE) LI-6400 Portable Photosynthesis System. Because all leaves measured were large, the area of leaf for which gas

PHOTOSYNTHETIC PLASTICITY IN EPIPHYTES exchange was measured matched the maximum area possible (6 cm2) in the gas exchange chamber. Photosynthetic parameters were measured two different ways at the central portion of each leaf: once with the adaxial surface illuminated and again adjacent to the same leaf location with the abaxial surface illuminated. The exact same location on the leaf was not used for both measurements to ensure that manipulation by inserting the leaf into the chamber and clamping the chamber on the leaf for the first measurement did not influence the second measurement. Although gas exchange was always measured for both sides of the leaf simultaneously, the chamber was oriented such that only the adaxial or abaxial surface received light from the blue and red diodes in the top half of the chamber. Very little ambient light reached the opposing leaf surface during the measurements as a result of shading by parts of the gas exchange chamber, the investigators, and nearby vegetation. Photosynthesis was measured three times with illumination on one surface of a leaf at a low PPFD (100 µmol m-2 s-1), then three times at a high PPFD (1000 µmol m-2 s-1) Using the same leaf, the chamber was then reversed to measure gas exchange with illumination (both PPFD levels) on the opposite -2 -1 leaf surface. Net CO2 uptake in A. nidus saturated at approximately 500 µmol m s (determined with preliminary gas exchange measurements). Other environmental conditions during all measurements were maintained by the LI-6400 system at the following values: air -1 CO2 concentration of 370 µmol mol , chamber (“block”) temperature of 30°C (leaf temperatures were typically 0.5° C higher), vapor pressure deficit (vpd) of 0.9 mbar, and flow rate of 200 μmol s-1. Lower vpd values resulted in exceedingly low transpiration rates, which led to unrealistic values for Ci; any such data were discarded. For each gas exchange measurement, data were recorded only when gas exchange rates were stable (Coefficient of Variation of exchange rates of both gases and flow rates not varying by more than 0.2% among successive measurements every 2-3 seconds), typically within 10 seconds of inserting the leaf in the gas exchange chamber or after the previous measurement (for a total of three repeated measurements). The gas exchange chamber remained clamped to a leaf for approximately five minutes at each light level, allowing for stable readings, as well as steps taken to ensure instrument accuracy (e.g., using the “match” function of the LI-6400 prior to each measurement).

Statistical analyses

Means of gas exchange parameters (N=5; the value for each plant being a mean of three repeat measurements; see above) for abaxial and adaxial surfaces at each light level were compared with a paired Student’s t-test when the data met the assumptions of parametric statistics (Sokal and Rohlf, 1981) or with a Mann-Whitney U-test otherwise.

CHAPTER 5

Results and discussion

The adaxial side of the vertical leaves growing out of the rosettes of A. nidus is unlikely to receive direct radiation due to shading by the host tree trunk, whereas the exposed abaxial side should at least occasionally intercept direct solar radiation. Thus, based on results with terrestrial plants (Syvertson and Cunningham, 1979; Terashima, 1989; DeLucia et al. 1991; Poulson and DeLucia 1993), it was predicted that the illumination of the abaxial side of the vertical leaves of A. nidus would result in higher photosynthetic rates than when the adaxial side of the same leaf is illuminated. Measurements of photosynthesis at both high and low PPFD of plants in northeastern Taiwan did not, however, support this prediction (Fig. 1). In contrast, although not statistically significant (high PPFD P= 0.28; low PPFD P = 0.17), the trend in the data indicated the opposite of expectations, i.e., photosynthetic rates at either PPFD appeared higher when the adaxial surface was illuminated. According to the statistical analyses, however, photosynthetic rates at both light levels were equal regardless of which side of the leaf was illuminated (Fig. 1).

Fig. 1 Mean (lines projecting from bars are standard deviations; n = 6 plants, three repeated measurements per leaf for each plant) rates of net CO2 exchange (positive values indicate CO2 uptake) for different leaves and with illumination at two light levels on either side of the leaves of the epiphytic fern Asplenium nidus measured in situ in a subtropical rain forest in northeastern Taiwan). Abbreviations for type and side of leaf are: “VR” = vertical, “HZ” = horizontal, “AN” = angled (45° from vertical); and “AD” indicates illumination (A, 100 µmol m‐2 s‐1; B, 1000 µmol m‐2 s‐1) provided to the adaxial side of the leaf during gas exchange measurements; “AB” indicates illumination (low and high PPFD as in AD) provided to the abaxial side of the leaf during measurements. The abaxial and adaxial means for two leaves at low PPFD are significantly different at P < 0.05 or P < 0.01 indicated by “*” or “**”, respectively, above each pair of means, while the other pairs of means are not significantly different (P > 0.05, indicated by “ns” above each pair of means).

PHOTOSYNTHETIC PLASTICITY IN EPIPHYTES Net H -1 s 2 -2 O Exchange, mmol m mmol Exchange, O 0.4 ns A B 4 ns ns 0.3 ns 3 ns ns 0.2 2

0.1 1 O Exchange, mmol m O Exchange, mmol 2 0.0 0 -2 VRAD VRAB HZAD HZAB ANAD ANAB VRAD VRAB HZAD HZAB ANAD ANAB s -1

Net H Leaf Type & Side Leaf Type & Side

Fig. 2 Mean (lines projecting from bars are standard deviations; n = 6 plants, three repeated measurements per leaf for each plant) rates of net H2O exchange (positive values indicate water vapor loss) for different leaves and with illumination at two light levels on either side of the leaves of the epiphytic fern Asplenium nidus measured in situ in a subtropical rain forest in northeastern Taiwan). Abbreviations for type and side of leaf are: “VR” = vertical, “HZ” = horizontal, “AN” = angled (45° from vertical); and “AD” indicates illumination (A, 100 µmol m‐2 s‐1; B, 1000 µmol m‐2 s‐1) provided to the adaxial side of the leaf during gas exchange measurements; “AB” indicates illumination (low and high PPFD as in AD) provided to the abaxial side of the leaf during measurements. None of the abaxial and adaxial means at any leaf location are significantly different (P > 0.05, indicated by “ns” above each pair of means).

Light interception of the two surfaces of the horizontal leaves of the epiphytic fern A. nidus is quite different from that of the vertical leaves, and the prediction of comparative photosynthetic capacities when the two sides of this leaf are illuminated is the opposite of that of the vertical leaves of this fern. Because the adaxial surfaces of these leaves intercept more direct solar radiation than do the abaxial surfaces, photosynthetic rates when the adaxial surface of the horizontal leaves of this epiphyte are illuminated should be higher than those of the leaf when the abaxial surface of the same leaf is illuminated. Measurements of photosynthetic rates confirmed this prediction, although the higher photosynthetic rates when the adaxial side of the leaves was illuminated, were statistically significant only when measurements were made at the lower PPFD (Fig. 1). These higher net CO2 uptake rates were accompanied by equal transpiration rates (Fig. 2) and stomatal conductances (Fig. 3), while internal CO2 concentrations were significantly lower (Fig. 4). These gas exchange results indicate that the higher photosynthetic rate was most likely the result of a greater biochemical capacity for photosynthesis and not the result of greater stomatal opening and, hence, easier gas diffusion into the leaf (Farquhar and Sharkey, 1982; Sharkey, 1985). In agreement with the latter interpretation, it is possible, especially for the measurements made at high light, that

CHAPTER 5 illumination of the abaxial surface resulted in photoinhibition in this lateral half of the section of leaf being measured. This possibility is supported by previous findings that the side of a leaf that is typically less exposed to sunlight has chloroplasts and photosynthetic features typical of shade-adapted leaves (Schreiber et al., 1977; Kulandaivelu et al., 1983; Terashima and Inoue, 1984; Terashima et al., 1986). Differences in photosynthetic capacity depending on which side of the leaf is illuminated might also reflect other anatomical or optical (e.g., absorptance) features of the two sides of the leaf (Terashima 1986; DeLucia et al., 1991). Such differences would also be interpreted as non-stomatal and non-diffusional mechanisms responsible for differences in photosynthesis between the two sides of the leaf, as was found in this study.

Conductance,m mol -1 ns 4 s 0.4 -2 ns ns A B

0.3 3 * ns * 0.2 2

0.1 1 -2 s -1 Conductance, molm 0.0 0 VRAD VRAB HZAD HZAB ANAD ANAB VRAD VRAB HZAD HZAB ANAD ANAB Leaf Type & Side Leaf Type & Side

Fig. 3 Mean (lines projecting from bars are standard deviations; N = 6 plants, three repeated measurements per leaf for each plant) stomatal conductances for different leaves and with illumination at two light levels on either side of the leaves of the epiphytic fern Asplenium nidus measured in situ in a subtropical rain forest in northeastern Taiwan). Abbreviations for type and side of leaf are: “VR” = vertical, “HZ” = horizontal, “AN” = angled (45° from vertical); and “AD” indicates illumination (A,100 µmol m‐2 s‐1; B, 1000 µmol m‐2 s‐1 in Fig. 3B) provided to the adaxial side of the leaf during gas exchange measurements; “AB” indicates illumination (low and high PPFD as in AD) provided to the abaxial side of the leaf during measurements. The abaxial and adaxial means at two leaf locations at high PPFD are significantly different at P < 0.05, indicated by “*” above each pair of means, while the other pairs of means are not significantly different (P > 0.05, indicated by “ns” above each pair of means).

PHOTOSYNTHETIC PLASTICITY IN EPIPHYTES

Fig. 4 Mean (lines projecting from bars are standard deviations; N = 6 plants, three repeated measurements per leaf for each plant) leaf internal CO2 concentrations (external CO2 concentration was 370 µmol mol‐1 ) for different leaves and with illumination at two light levels on either side of the leaves of the epiphytic fern Asplenium nidus measured in situ in a subtropical rain forest in northeastern Taiwan). Abbreviations for type and side of leaf are: “VR” = vertical, “HZ” = horizontal, “AN” = angled (45° from vertical); and “AD” indicates illumination (A, 100 µmol m‐2 s‐1; B,1000 µmol m‐2 s‐1) provided to the adaxial side of the leaf during gas exchange measurements; “AB” indicates illumination (low and high PPFD as in AD) provided to the abaxial side of the leaf during measurements. The abaxial and adaxial means at several leaf locations are significantly different at P < 0.05 or P < 0.01, indicated by “*” or “**”, respectively, above each pair of means, while the other pairs of means are not significantly different (P > 0.05, indicated by “ns” above each pair of means).

Both the adaxial and abaxial surfaces of the “angled” leaves of A. nidus should intercept direct sunlight, at least for brief periods, throughout a day. Thus, one might predict that the photosynthetic capacity of these leaves is comparable, regardless which surface is illuminated (Syvertsen and Cunningham, 1979; Václavík, 1984; DeLucia et al., 1991; Poulson and DeLucia, 1993). Based on measurements made in situ with this epiphytic fern in northeastern Taiwan, this prediction was supported when gas exchange was measured at high PPFD (Fig. 1), but the photosynthetic rate when the adaxial leaf surface was illuminated exceeded that when the abaxial surface of the leaf was illuminated at low PPFD (Fig. 1). As was the case with the horizontal leaves, the higher net CO2 exchange rate of the angled leaves was apparently the result of a greater biochemical capacity for photosynthesis, generating a lower leaf internal CO2 concentration (Fig. 4), and not due to a greater stomatal conductance (Fig. 3; Farquhar and Sharkey, 1982; Sharkey, 1985). These findings contrast directly with those for Sitka spruce by Leverenz and Jarvis (1979), who found that differences in photosynthetic capacity of the leaves, depending on which side of the leaf was illuminated could be ascribed to differences in stomatal conductance, not to the biochemical capacity of the leaf.

CHAPTER 5

Overall, the results of in situ gas exchange measurements with A. nidus in a subtropical rain forest in northeastern Taiwan lend considerable, but not complete, support to past findings with terrestrial taxa (Syvertsen and Cunningham, 1979; Terashima, 1989; DeLucia et al., 1991; Poulson and DeLucia, 1993). In most, but not all, cases, if a leaf is oriented such that one side receives more direct solar radiation than the other, the leaf has a higher photosynthetic capacity when the more exposed surface is illuminated. In addition, this higher capacity reflects a greater biochemical capacity for photosynthesis and not easier diffusion of

CO2 into the leaf (Farquhar and Sharkey 1982; Sharkey, 1985).

Chapter 6 Adaptation of a widespread epiphytic fern to simulated climate‐change conditions

A. antiquum sporelings were transplanted to each of the sites where the spores were collected. Young ferns were planted in paper tea bags filled with peat moss, which were fixed to a 40 ×50 cm coconut mat. The mats, 10 per site, were nailed to a tree trunk at eye‐level height.

CHAPTER 6

Adaptation of a widespread epiphytic fern to simulated climate-change conditions

Rebecca C.-C. Hsu, J. Gerard B. Oostermeijer & Jan H.D. Wolf

Abstract

The response of species to climate change is generally studied using ex situ manipulation of microclimate or by modeling species range shifts under simulated climate scenarios. In contrast, a reciprocal transplant experiment was used to investigate the in situ adaptive response of the elevationally widespread epiphytic fern Asplenium antiquum to simulated climate change conditions. Fern spores were collected at three elevations and germinated in a greenhouse. The sporelings (juvenile ferns) were reciprocally transplanted to each collection site. Growth and mortality rates were monitored for two years. Wild sporelings were monitored at two sites to assess possible transplant effects. Habitat suitability, indicated by overall growth and survival patterns, declined as elevation increased. Only the highland population showed significant adaptation to the ‘home’ habitat, achieving the highest survival rates. Microclimate data suggests that the presumed genetic adaptation at the highland site occurred mainly in response to drought stress in winter. Based on our previous study on species distribution models, which projected an expansion in the range of A. antiquum under future climate change scenarios, the populations at the upper margins of the species’ elevational range may play an important role during this expansion, given their improved adaptation to the shifting marginal conditions. The study suggests that intraspecific variation should be considered when establishing the potential impact of climate change on biodiversity.

Introduction

The response of species to global climate change is of great interest in conservation biology. Vulnerability to climate change differs among biomes and is related to the ecological and genetic properties of species (Root et al., 2003; Broennimann et al., 2006; Loarie et al., 2009). Under changing climate conditions, inferred responses include phenotypic plasticity, genetic adaptation and migration, and the most dramatic consequence is species extinction. Phenotypic plasticity is the ability of a genotype to exhibit variable phenotypes in response to environmental change, whereas genetic adaptation is an evolutionary process, during which selection favours individuals with novel gene and allele combinations that either arise by sexual recombination or by immigration from other populations (Nicotra et al., 2010). Adaptation and

EPIPHYTE ADAPTATION TO CLIMATE CHANGE phenotypic plasticity contribute to the ecological amplitude of a species if populations occur in diverse habitats, and may permit populations to persist in spatially and temporally heterogeneous environments (Silander 1985). Besides the capacity for dispersal and establishment, the extent of adaptation may well determine the vulnerability of a species to climate change (Hedderson and Longton 2008).

Widespread species (generalists) occur across a broad range of environmental gradients and thus usually comprise several climatically-adapted populations (ecotypes). Hence, generalist species are likely to demonstrate broader tolerances to climate change than specialists that are geographically restricted (Broennimann et al., 2006; Aitken et al., 2008). The identification of ecotypes of economically important plants that are genetically adapted to future climates is viewed as a promising strategy for sustainable agriculture in the face of climate change (Kreyling et al., 2012). The favored traits under climate changes could be identified by comparing selection regimes in current environments to those in environments similar to predicted future conditions, (Etterson 2004). However, climate change impacts on species adaptability have been explored for only very few species. Therefore, population studies on the genetic adaptation and phenotypic plasticity of species in relation to climate change deserve special attention.

Epiphytes are presumed to be particularly sensitive to climate change since they have no vascular connection to the ground or their host plants. They solely rely on the contact with rain or cloud droplets for moisture input, hence respond rapidly to slight changes in ambient climate (Benzing 1998; Zotz and Bader 2009). Contrary to common expectation, our recent study (Hsu et al., 2012) using species distribution modeling (SDM) suggested that several species (e.g. Asplenium antiquum) would expand its range size under future A2 and B2 climate change scenarios (Nakicenovic et al., 2000). However, a general shortcoming of SDM is that it does not consider the possibility of intraspecific variation of the modeled species along climate gradients (Benito Garzón et al., 2011). Studies suggested when sub-taxon information (i.e. subspecies) was incorporated into SDM, the species was projected to better tolerate climate change (Pearman et al., 2010; Oney et al., 2013).

Reciprocal transplant experiments were previously conducted, using epiphyte mats (i.e. the combined unit of living epiphytic plants and associated detrital matter), to evaluate epiphyte sensitivity to manipulated climate-change conditions (Nadkarni and Solano 2002; Song et al., 2012). In this study, we reciprocally transplanted juveniles of a single species, Asplenium antiquum Makino, to three different elevations. The main aim of this study is to evaluate if altitudinally separated populations of A. antiquum are adapted to their local environment.

CHAPTER 6

Fig. 1 Locations of the three study sites within Taiwan. Circle: low elevation site at 600 m asl; diamond: mid elevation site at 1100 m asl; triangle: high elevation site at 1950 m asl.

EPIPHYTE ADAPTATION TO CLIMATE CHANGE

Materials and Methods

Study species

A. antiquum is a widespread epiphytic fern native to China, Japan, Korea and Taiwan. Its common name, ‘bird’s nest fern’, is derived from its rosette growth form, which traps fallen leaves and other debris. Adult plants may reach 300 cm in diameter (pers. observation). The clumped plant bases are composed of fibrous roots and trapped humus, which sponge up rainwater to facilitate successful establishment in the forest canopy. A. antiquum is the elevationally most widespread species, ranging from the coast to up to c. 2500 m above sea level [asl], among the three species of bird’s nest ferns in Taiwan.

Study sites

We selected three remote sites in primary broad-leaved forests with thriving populations comprising several hundreds of adult A. antiquum plants for spore collection and the reciprocal transplant experiment. The sites were located at Fushan (lowland, 600 m asl), SiangBenShan (midland, 1100 m asl) and PeiTungYenShan (highland, 1950 m asl) (Fig. 1). The horizontal distances between the lowland and the midland and between the midland and the highland sites were 39 km and 50 km, respectively. The lowland and midland sites are in north-eastern Taiwan and dominated by Lauraceae trees (e.g. Machilus zuihoensis, Litsea acuminata, Machilus japonica, Phoebe formosana) with an average height of 15 m. The highland site is situated at the west side of the island central ridge, with a higher canopy (c. 20 m, dominant trees: Schima superba and Castanopsis carlesii) than the two lower sites.

Climate measurements

The average annual rainfall recorded at the lowland, midland and highland sites is c. 3500, 3800 and 2500 mm, respectively (Central Weather Bureau). At each site we placed two data loggers (model U23-001, HOBO Pro V2 Temp/RH Data logger, Onset computer corporation, Bourne, MA, USA), and one visibility meter (model MiniOFS, Sten Löfving Optical Sensors, Göteborg, Sweden) to record local temperature and relative humidity per hour and fog events every 30 minutes during the course of the experiment. In addition, we recorded the phenology of three adult A. antiquum individuals per site at monthly intervals.

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Fig. 2 Monthly mean temperature recorded at three elevation sites from Dec 2008 to Dec 2010. Bars indicate the monthly maximum and minimum temperatures being recorded. L: low elevation site (600m asl); M: mid elevation site (1100m asl); H: high elevation site (1950 m asl).

Reciprocal transplant experiment

In November 2007, fertile leaves of ten A. antiquum individuals were sampled haphazardly with a 5-m branch cutter from each of the three elevational sites and air-dried to collect the spores. In January 2008, spores were bulked and germinated on sterilized soil in covered plastic boxes. After six months, sporelings were replanted on Sphagnum peat substrate. In December 2008, one-year-old sporelings were transplanted to each of the sites from which the spores were collected, coinciding with the beginning of the north-eastern monsoon that brings rainwater to help establish the plants. Nevertheless, all sporelings transplanted at the highland site died in the first month due to very low moisture levels. Therefore, a second batch of sporelings from the same bulked spore sample that had been germinated as backup in July 2008 was re- transplanted in July 2009 to the highland site. Young ferns were planted in paper tea bags filled with peat moss, which were fixed to a 40 × 50 cm coconut mat. The mats, 10 per site, were nailed to a tree trunk at eye-level height, with 15 bags containing one plant each (i.e. five plants per altitudinal origin). All transplants were randomly allocated a place on the mat; in total, there were 50 sporelings per origin per location. The diameter and mortality of the transplanted sporelings were recorded in the field each month. Dead and missing (due to animals, wind and heavy rain) plants were tallied separately, based on their health condition at previous month’s visit. Wild sporelings were also monitored at the high and low elevation sites that are relatively environmental distinctive to assess possible transplant effects. A batch of sporelings planted in

EPIPHYTE ADAPTATION TO CLIMATE CHANGE pots was kept in a nursery. At the end of the experiment, their diameter was measured before they were dried in an oven at 65 °C to assess the correlation between diameter and biomass.

Data analysis

A regression analysis was performed to test the correlation between the rosette diameter and the dry weight (biomass) of the sporelings. The growth of local and foreign sporelings at each site was compared using the relative growth rate, RGR (Hunt 1982), calculated using the following equation:

RGR = (ln(D2) – ln(D1))/(t2 – t1) in which D1 and D2 are plant diameters (mm) at times t1 and t2 (days).

Overall differences in mean RGR (i.e. averaged RGR for each individual sporeling between visits) and final sporeling size among populations were tested with two-way ANOVA, using initial size as covariate, to test effects of elevation, sporeling origin and the elevation-by-origin interaction. The smaller second batch of transplanted sporelings at the high elevation site was excluded from the final size comparison among sites. Mean sporelings’ RGR between visits were correlated with local microclimates (i.e. mean temperature and relative humidity). Because temperature and humidity were not independent, we calculated partial correlation coefficients, controlling for one or the other variable. We tested the success of sporeling settlement at the three elevations using Kaplan-Meier survival analysis (Kaplan and Meier 1958), and compared the survival curves of populations among and within sites with a log rank test (Bland and Douglas 2004). All analyses were performed using SPSS (version 13.0, IBM).

Results

Climate at study sites

Our climate dataloggers showed that mean temperatures decreased from the lowland to the midland and highland site, having an annual mean temperature (± SE.) of 17.3 (4.27), 15.7 (4.35) and 13.1 (3.43) °C, respectively (Fig. 2). Unexpectedly, during the course of the experiment, the temperature occasionally dropped below zero at the lowland site. The annual mean diurnal temperature (i.e. the difference between daily maximum and minimum temperature) ranged between 5.79 (1.17), 3.87 (0.2) and 5.57 (0.9) °C from the lowland to the highland site, respectively. Monthly mean air humidity significantly decreased from the lowland to the highland site (Fig. 3, ANOVA, p < 0.001). During the experimental period, the lowland and midland sites were relatively dry in late spring (May), whilst the highland was quite dry in the winter (Fig. 3). The frequency of mist (1 km < visibility < 2 km) and fog (visibility < 1 km)

CHAPTER 6 events also varied between the three sites. Foggy conditions were most frequent in the midland site (1667 hrs/ year) in comparison to the lowland (116 hrs/ year) and highland (754 hrs/ year) sites. In contrast to regular afternoon fogs at mid and high elevation sites, morning mist was relatively common at the low elevation site, a typical characteristic of tropical lowland cloud forest (Gehrig-Downie et al., 2011).

Table 2 Results of partial correlation analysis between the RGR of A. antiquum sporelings and local microclimate (mean temperature and relative humidity of between‐visit duration) at three transplant sites from Dec 2008 to Dec 2010. For comparison, data were also pooled to calculate (a) single and (b) partial correlation coefficients. T = mean temperature, RH = relative humidity; low elevation: 600 m asl, mid elevation: 1100 m asl and high elevation: 1950 m asl. Numbers in brackets indicate p values.

Correlated Correlation coefficient (Controlling) Source factors Lowland origin Midland origin Highland origin

Site 0.265 (0.094) 0.406 (0.008)*** 0.265 (0.094) pooled (a) Sites T 0.183 (0.266) 0.247 (0.124) 0.144 (0.377) pooled (b) Low (RH) 0.68 (0.015)** 0.723 (0.005)*** 0.506 (0.078) elevation Mid 0.223 (0.464) 0.527 (0.064)* 0.435 (0.137) elevation High ‐0.114 (0.724) ‐0.502 (0.096) ‐0.201 (0.53) elevation Site 0.252 (0.113) 0.492 (0.001)*** 0.333 (0.033)** pooled (a) Site RH 0.132 (0.424) 0.385 (0.014)** 0.251 (0.118) pooled (b) Low (T) 0.229 (0.452) ‐0.536 (0.059)* 0.513 (0.073)* elevation Mid ‐0.072 (0.814) 0.568 (0.043)** 0.631 (0.021)** elevation High 0.15 (0.642) 0.604 (0.038)** 0.222 (0.488) elevation Codes for significance: *** p < 0.01, ** p < 0.05, * p < 0.1.

EPIPHYTE ADAPTATION TO CLIMATE CHANGE

Fig. 3 Monthly mean air humidity at three elevation sites from Dec 2008 to Dec 2010. L: low elevation site (600m asl); M: mid elevation site (1100m asl); H: high elevation site (1950 m asl).

Plant phenology, growth and survival

At the lowland and midland sites, the monitored adult ferns produced new leaves in early spring (February to March), and there was a second budding in autumn (September), yet the plants produced no sporangia. At the highland site, new leaves appeared only once a year, during the spring rain period in April. Although, sporeling growth estimated as diameter increase varied greatly among different origin sites, the diameter of the sporelings was significantly correlated with their dry weight, for sporelings of the same origin as well as for all sporelings combined (Fig. 6).

After correcting for a significant effect of initial sporeling size (i.e. larger transplants grew faster), the average RGR was significantly lower at the highest elevation (F(2, 78) = 22.1, p < 0.001, Table 1). The origin of sporelings had no significant effect on the average RGR, but there was an elevation-by-origin interaction (F(4,78) = 3.11, p = 0.02). Separate analyses for each elevation showed a significant origin effect on RGR (F(2,49) = 3.98, p = 0.025) only at the low elevation site (Table 1). Sporelings’ average final sizes were 57.26 (27.5), 58.81 (33.04) and 19.02 (9.30) mm (± SE.) at low, mid and high elevations, respectively (Fig. 5). Between the low and mid elevation sites, sporelings’ final sizes were similar (F(1, 69) = 0.259, p = 0.612, Table 1). However, the second batch of transplant sporelings at the high elevation site (i.e. a half year

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younger) were significantly smaller than those at the other two sites (F(2,78) = 7.468, p = 0.001). Moreover, the origin of sporelings only had a marginally significant effect on the final size at the low elevation (F(2,78) = 2.68, p = 0.079). This was mainly caused by a lower RGR (Fig. 4) and smaller size (Fig. 5) of the highland sporelings. The wild sporelings generally had the same growth pattern with transplanted plants (Fig. 5), suggesting the external (climatic) environmental exert more influence on growth than transplant effect.

Fig. 4 Comparison of sporelings' mean RGR from Dec 2008 to Dec 2010 among three elevation sites. Bars indicate ± SE. Different letters (a, b, c) indicate significant difference at p < 0.05 (ANOVA). L: lowland sporelings (circle); M: midland sporelings (diamond); H: highland sporelings (triangle).

EPIPHYTE ADAPTATION TO CLIMATE CHANGE

Fig. 5 Growth (represented by average rosette diameter) of transplanted and wild local sporelings of A. antiquum from Dec 2008 to Dec 2010 at three elevation sites. Wild sporelings were monitored for comparative purposes at the low and high elevation sites. Bars indicate ± SE. L: lowland sporelings; M: midland sporelings; H: highland sporelings; W: wild sporelings.

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Fig. 6 Regression analysis of the biomass‐diameter relationship of A. antiquum sporelings cultivated in a nursery for two years. The exponential equation is fitted for samples originating from three elevation sites. L: lowland sporelings (circle); M: midland sporelings (diamond); H: highland sporelings (triangle).

The results suggested that temperature explained most of the variation in RGR at the low-elevation site, whereas the RGR was correlated mainly with relative humidity at both the mid and high elevation sites (Table 2). The RGR of lowland origins were only correlated (p = 0.015) with temperature at the low elevation site. For highland origins, air humidity was significant correlated with their RGR at the mid elevation site (p = 0.021), and was marginally correlated at the low elevation site (p = 0.073). The midland origins showed the highest sensitivity to microclimates among sites, and demonstrated a significant correlation (p = 0.005) with air temperature at the low elevation site.

EPIPHYTE ADAPTATION TO CLIMATE CHANGE

Fig. 7 Kaplan‐Meier survival curves of reciprocally transplanted A. antiquum sporelings originating from three elevations, grouped by transplantation sites. L: lowland sporelings (circle); M: midland sporelings (diamond); H: highland sporelings (triangle).

Across origins, the survivorship of sporelings was significantly affected by elevation, and to some extent, by origin within some elevations (Fig. 7). Mean sporeling survival was highest at the low elevation site (50%), followed by the mid (22.3%) and high elevation (10.3%) sites (Mantel-Cox log-rank test, Chi-square = 119.1, df = 2, p ≤ 0.001). Across elevations, mean survival of sporelings from all three origins was largely similar, although marginally better for highland sporelings (23.8% for lowland, 16.1% for midland and 34% for highland sporelings; Chi-square = 5.0, df = 2, p = 0.084). At the low elevation, the highland sporelings survived significantly better (70%) than the lowland (50%) and midland (28%) sporelings (Chi-square =

CHAPTER 6

6.4, df = 2, p = 0.040). At the mid elevation site, the survival rates were not significantly different among origins (lowland: 24.3%, midland: 22.6% and highland: 20.0%; Chi-square = 1.06, df = 2, p = 0.590). At the high elevation, the highland sporelings survived significantly better (20%) than the midland (2.7%) and lowland sporelings (7.1%) (Chi-square = 16.2, df = 2, p ≤ 0.001). Hence, an advantage for ‘home’ sporelings only existed at high elevations, but these highland sporelings also survived better at low elevation, where they grew less and slower than sporelings from the other two origins (Fig. 4, 5).

Discussion

The climatic differences between the three elevations were largely in accordance with expectations for wet subtropical mountains (Walter 1985). Average daily temperatures dropped with elevation. However, we recorded frost (daily minimum temperature < 0°C) not only at the high elevation site but also at the low elevation site even in March. In comparison with the mid elevation site, the low elevation site exhibited a relatively high seasonal and diurnal temperature range. This pattern appears to be induced by variation in local topography and associated regional climates. The low elevation site, situated in north-eastern island, is intensively influenced by NE-monsoon in winter. NE-monsoon generally accounts for 45% of the total annual rainfall in eastern Taiwan (Kao et al., 2004) and occasionally causes frost events in early spring. For example in 2005, a relatively warm winter followed by a severe frost event in March led to extensive second budding and re-foliating of plants in northern Taiwan. On the contrary, the mid elevation site demonstrated less variation in temperature, which probably can be attributed to its high frequency of fogs and associated reduced thermal radiation, a characteristic of montane cloud forests worldwide (Jarvis and Mulligan 2011). The lowest mean relative humidity occurred at the high elevation. Unlike the lowland and midland sites that receive large amounts of monsoon rainfall in winter, the highland site is only slightly influenced by the NE-monsoon for its location on the west side of the central ridge. In agreement, we observed wrinkled fronds of adult A. antiquum plants in winter during the study period. Moreover, we noticed delayed leaf budding at the highland site that may also be related to water deficiency, since rapid elongation of fronds requires sufficient water (Freiberg and Turton 2007). Low water availability at the high elevation site presumably accounted for the failure of the first transplant experiment in Dec 2008.

It is also likely that the variation in climate between the elevational sites affected the growth and survivorship of the A. antiquum sporelings. To estimate growth during the course of the study, we measured the diameter of the plants in a non-destructive way. The significant diameter-biomass correlation showed that the diameter of A. antiquum rosettes may be used to measure individual growth. We found that site (elevation) had a significant effect on the final transplant size, the relative growth rate (RGR) and the survival rate of sporelings. From low to

EPIPHYTE ADAPTATION TO CLIMATE CHANGE high elevation, the RGR decreased and the mortality increased. Growth rates were significantly positively correlated with both temperature and relative humidity, especially for midland sporelings that originated in the mid elevation site with a relatively stable microclimate. When controlling for the correlation between these variables, we found that temperature had the greatest influence on RGR variation at the low elevation site, but at the mid and high elevation sites, relative humidity had the greatest influence. We postulate that the high mortality at the high elevation site is better explained by low water availability rather than reduced temperature, since sporelings at the low elevation site also experienced low temperatures, even frost, but showed higher survivorship than those at the highland site. Based on differences in final size, RGR and mortality of sporelings among sites, we conclude that the warm low elevation site with prolonged moisture availability was the most suitable habitat for A. antiquum sporelings in this study, whereas the high elevation site appeared to impose a more intense selection pressure, mostly through drought stress in the winter.

Our study showed that significant differences among elevations occurred in A. antiquum phenology, sporeling growth and mortality. Although the lack of replication among elevations (owing to poor site accessibility) does not allow us to conclusively link these differences to the elevation-specific climate conditions, the patterns observed suggest that such links exist. At the high elevation site, the higher survivorship of local sporelings as compared to the foreign ones (from lowland and midland origins) suggests a certain degree of genetic adaptation, resulting in higher tolerance to drought stress and low temperatures. The highland sporelings also had higher survivorship than the local and midland plants at low elevation, which suggests that their significantly slower growth rates were partly adaptive. Slow growth, a trait that is advantageous at high altitude (Oleksyn et al., 1998; Macek et al., 2009) was maintained by highland sporelings at low elevations, indicating a genetic basis. Although normally a disadvantage at lower elevations, a reduced RGR may have given them an advantage under the extreme conditions encountered during the experiment (such as frost). The advantage of highland sporelings during frost events at the low elevation site might have been accidental. Slower growth might also have been beneficial to survive the transplantation from greenhouse to the field (Wright et al., 2010). Generally though, the higher RGR of lowland sporelings should increase their fitness at the relatively warm and humid low elevations.

Our experiment has shown that there seems adaptive genetic differentiation among populations of A. antiquum growing at different elevations, even though we expected that the generally high dispersal ability of fern spores would prevent such differentiation. Regarding gene flow, previous research has identified a high level of genetic differentiation in A. antiquum at a larger spatial scale, namely within East Asia (Murakami et al., 1999). In West Java, the closely-related A. nidus, a species likely to have similar patterns of spore dispersal and thus gene

CHAPTER 6 flow as A. antiquum, was observed to have separate rbcL-haplotypes that were clearly linked to different elevations (Yatabe et al., 2002). A. nidus was also reported to have a diverse height of attachment and habitat preference (hills versus swamps) for individuals of different sizes in peninsular Malaysia, which was attributed to the existence of cryptic species (Zhang et al., 2010). Supported by our experimental results, the literature suggests that a genetic differentiation of A. antiquum among different elevations is likely. The differentiation is probably driven by adaptation to the more extreme climate conditions at high elevations that led to selection favouring slower growth and conservative use of resources. This selection appears to be sufficient to counter any ‘diluting’ effects of gene flow from populations at lower elevations (Gonzalo-Turpin and Hazard 2009).

Comparing this with the projected distributions of A. antiquum under climate change scenarios (Hsu et al., 2012), we found that the greatest range expansion occurred in the south- eastern lowlands (both A2 and B2 scenarios) and at higher elevations (A2 scenario, with high rainfall increase). Like most species distribution models, our initial model assumed unlimited dispersal. Based on these experimental results, we conclude that dispersal is poorer than expected for the small lightweight spores. For the above-mentioned projected distributions, we deduce that colonization to higher altitudes would occur mainly through the genetically preadapted highland populations, whereas expansion into lower altitudes would be best achieved by rapid-growing plants from lowland (and midland) populations. Thus, A. antiquum is not expected to be negatively affected by climate change, owing to its wide distribution and genetic adaptation at its range margin. However, some caution is in order, since we have only considered sporeling growth and survival and have no data on the performance (e.g. growth, mortality and reproduction) of adult plants or the establishment of the sporelings in situ (i.e. germination and attachment).

In conclusion, our reciprocal transplant experiment showed a strong site effect on both the growth and survivorship of juvenile A. antiquum, indicating that habitat suitability differed substantially between the sites. At the more extreme climate conditions observed at the high elevation site, the local plants were clearly better adapted, evidenced by their higher survival. These highland plants also grew more slowly but survived more successfully at the low elevation site. This may be an accidental consequence of the frost event that we recorded during our experimental period, to which the highland sporelings were probably better adapted. Under normal lowland conditions, frost will be rare and faster growth will probably be advantageous, resulting in higher fitness. The present study demonstrates an integrated approach to assess the biodiversity consequence of climate change. The field studies on phenotypic plasticity and patterns of intraspecific adaptation provide complementary information which is valuable in parameterizing statistical distribution models.

Chapter 7 Simulating climate change impacts on forests and associated vascular epiphytes in a subtropical island of East Asia

Cypress forest is characterized by cool temperatures, continuously moist and dim conditions, typically enveloped in clouds during the afternoon. Many epiphytes with restricted distributions are specialized to this particular thermal Pleione formosana and hydrological regime.

CHAPTER 7

Simulating climate change impacts on forests and associated vascular epiphytes in a subtropical island of East Asia

Rebecca C.-C. Hsu, Wil L.M. Tamis, Niels Raes, Geert R. de Snoo, Jan H.D. Wolf, Gerard Oostermeijer & Shu-Hua Lin

Diversity and Distributions 18, no. 4 (2012): 334-347

Abstract

A hierarchical modelling approach incorporating forest migration velocity and forest type- epiphyte interactions with classical SDMs was used to model the responses of eight forest types and 237 vascular epiphytes for the year 2100 under two climate change scenarios. Forest distributions were modelled and modified by dominant tree species’ dispersal limitations and hypothesized persistence under unfavourable climate conditions (20 years for broad-leaved trees and 50 years for conifers). The modelled forest projections together with 16 environmental variables were used as predictors in models of epiphyte distributions. A null method was applied to validate the significance of epiphyte SDMs and potential vulnerable species were identified by calculating range turnover rates. For the year 2100, the model predicted a reduction in the range of most forest types, especially for Picea and cypress forests, which shifted to altitudes ca. 400 and 300 m higher, respectively. The models indicated that epiphyte distributions are highly correlated with forest types, and the majority (77–78%) of epiphyte species were also projected to lose 45–58% of their current range, shifting on average to altitudes ca. 400 m higher than currently. Range turnover rates suggested insensitive epiphytes were generally lowland or widespread species, whereas sensitive species were more geographically restricted, showing a higher correlation with temperature-related factors in their distributions. The hierarchical modelling approach successfully produced interpretable results, suggesting the importance of considering biotic interactions and the inclusion of terrain-related factors when developing SDMs for dependant species at a local scale. Long-term monitoring of potentially vulnerable sites is advised, especially of those sites that fall outside current conservation reserves where additional human disturbance is likely to exacerbate the effect of climate change.

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES

Introduction

Numerous studies indicate that climate change has already altered global patterns of biodiversity by modifying the geographical distributions of species (Root et al., 2003; Walther et al., 2005; Lenoir et al., 2008; Harsch et al., 2009; Woodall et al., 2009). In the field of climate change impact research, species distribution models (SDMs) or ecological niche models (ENMs) have been increasingly used to estimate potential species range shifts under paleontological and/or future climate change conditions (Bakkenes et al., 2002; Broennimann et al., 2006; Hijmans and Graham, 2006; Thuiller et al., 2006; Fitzpatrick et al., 2008; Jensen et al., 2008; Carnaval and Moritz, 2008). SDMs attempt to recognize species’ realized niche, which is used to construct potential geographic distributions by relating species occurrences with values of predictor variables across a series of observation sites (Guisan and Thuiller, 2005). However, purely climate-based models have been criticized in numerous studies because they may not contain sufficient environmental parameters to assess climate change impacts (Heikkinen et al., 2006; Austin and Van Niel, 2011a, b). For example, SDMs tend to overestimate the area of suitable habitats, particularly for those species with a strong dependency on other species (Huntley et al., 2010).

In wet tropics, epiphytes form a conspicuous layer in the forest canopy, and are regarded as one of the groups most vulnerable to global climate change (Benzing, 1998; Nadkarni & Solano, 2002; Zotz and Bader, 2009). Canopy-dwelling plants have no vascular connection to the ground or their host plants, making them more sensitive to environmental changes than their soil-rooted counterparts (Benzing, 2004). Two decades of monitoring the lichen flora of the Netherlands indicated a dramatic change on the species composition and abundance attributed to global warming (van Herk et al., 2002). Epiphyte performance relies on the presence and characteristics of host trees. Although exceptions exist (Callaway et al., 2002), most vascular epiphytes exhibit no clear host tree preference (Zimmerman and Olmsted, 1992; Hsu et al., 2002; Martin et al., 2007), yet, the host tree (phorophyte) composition has a significant influence on likely epiphyte assemblages (Benavides, 2010). Thus, assessing climate change impacts on epiphytes requires information on not only the regional climate, but also the microclimate associated with forest types and the specific epiphyte-tree biotic interactions. Studies have indicated that the inclusion of biotic interactions significantly improved the accuracy of SDMs (Leathwick et al., 1996; Araújo and Luoto, 2007; Preston et al., 2008). Other studies have pointed out that the rate of climate change probably outpaces the migration capacity of many species (Svenning et al., 2008; Thuiller et al., 2008). However, epiphytes are adapted to highly dynamic forest canopies by producing many, mostly wind-dispersed, seeds or spores (Benzing, 1990). Accordingly, the colonization of epiphytes on trees should be rapid, which, in addition to short life-cycles, makes epiphytes suitable climate change indicators 88

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(Lugo and Scatena, 1992). For other forest plants, it is still crucial to take dispersal limitation into account when simulating species distributions (Engler and Guisan, 2009); a study on Cape Proteaceae indicated that, even with an optimistic migration rate scenario, the modelled species range loss closely approximated null migration (Midgley et al., 2006). However, because it is difficult to obtain reliable dispersal data, especially for the tail end of the leptokurtic distribution, most studies assume either unlimited or no dispersal for the target species.

Fig. 1 Location and the contour altitudes of Taiwan. The Central Ridge runs north‐east to south along the island mountain chain.

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES

Other debates are concerned with species persistence in unfavourable climatic conditions (Loehle and LeBlanc, 1996). Common sense dictates that many species (especially long-lived trees) will not immediately perish during climate changes. Long-lived dominant canopy trees will be relatively resistant since they can tolerate years of slow growth, whilst early successional species will die rapidly if their growth rate falls below a minimum (Loehle and LeBlanc, 1996); this justifies the importance of including species persistence in SDMs. Despite aforementioned limitations, SDMs do provide valuable first-order assessments of potential climatic change impacts on biodiversity (Huntley et al., 2010). Pearson and Dawson (2003) suggested a hierarchical framework for modelling species distributions at different geographical scales in order to improve model reliability. We have also adopted this approach, and incorporated a number of non-climatic factors (such as topography).

This study aims to assess the climate change impacts on forests and vascular epiphytes in the subtropical island of Taiwan, using species distribution models. We propose a stepwise hierarchical modelling approach, and aim to improve model accuracy and realism by considering dispersal limitation, tree persistence and biotic interactions between epiphytes and host trees. Our study specifically addresses two questions: (1) How do environmental factors contribute to species distributions and their ecological interpretations? (2) What areas and which species are potentially vulnerable to climate change?

Methods

Study site, species collections and forest types

Taiwan (situated between 21°45'–25°56'N and 119°18'E–124°34'E) is an island with an area of 36,000 km2 (Fig. 1). About 70% of the island area is covered by mountains (> 1,000 m above sea level [asl]); Mt. Jade (3952 m) is the highest peak in Taiwan. The annual rainfall in Taiwan ranges from 1,000 mm to over 6,000 mm, and generally falls during the NE monsoon (October–January), spring rain (February–April), plum rain (May–June) and typhoon-induced heavy rain events (July–September). The NE monsoon accounts for 45% of the total annual rainfall, mainly in east Taiwan (Kao et al., 2004). Three hundred and thirty six species of vascular epiphytes have been reported for Taiwan (Hsu and Wolf, 2009), of which 271 species are holo-epiphytes (i.e. epiphytes that complete their entire life cycle without contacting the forest floor). In this study, we applied SDMs on those 271 strictly arboreal species to assess the impact of climate change under two projected scenarios.

Table 1 The eight forest types, associated characters and the maximum dispersal distance at target years.

Maximum Maximum Age of Forest type Altitudinal Persistence dispersal distance dispersal Dominant species Dispersal vector maturity (abbr. used) range (yr) 2 for persistence distance in (yr)1 trees (m)3 2100 (m) Lowland Ficus spp. Large canopy birds, 1 broad‐leaved <500 m 10 20 7759* 9699 Machilus spp. Macaques, Rodents forest (BLL) Midland Machilu spp. Large canopy birds, 2 broad‐leaved 500–1500 m 15 20 5173* 6466 Castanopsis spp. Macaques, Rodents forets (BLM) Highland Large canopy birds, 3 broad‐leaved >1500 m 20 20 3715* 4643 Quercus spp. Macaques, Rodents forest (BLH) Cypress Chamaecyparis 4 1800–2500 m Wind 30 50 1548** 3096 forest spp. 5 Pinus forest 800–3000 m Pinus taiwanensis Wind 15 50 3096** 6191 Tsuga chinensis var. 6 Tsuga Forest 2500–3200 m Wind 25 50 1857** 3715 formosana 7 Picea forest 2500–3200 m Picea morrisonicola Wind 30 50 1548** 3096 8 Abies forest >3200 m Abies kawakamii Wind 30 50 1548** 3096

1 USDA Forest Service (http://www.fs.fed.us/database/feis/plants/index.html); He and Mladenoff (1999); Verdú (2002); Engler and Guisan (2009). 2Engler and Guisan ( 2009). 3Maximum dispersal distance for the year 2080 (*) and 2050 (**).

We identified the locations of epiphytic species from herbarium records, published plant inventories and our own botanical observations. We assigned species occurrences to 1 km2 grid cells; multiple occurrences within the same cell were considered as one ‘unique’ record. The final database comprised 18,239 records (occurrences ranged from five to 1,083) including 237 species; 34 species with less than five unique localities were excluded from the model. Over 90% of modelled species were either ferns or orchids (see Appendix 2). According to the typology studies (Su, 1992; Chiou et al., 2009), the Taiwanese major forest types can be grouped as: (1) lowland broad-leaved forest (BLL), (2) midland broad-leaved forest (BLM), (3) highland broad-leaved forest (BLH), (4) cypress forest, (5) Pinus forest, (6) Tsuga forest, (7) Picea forest and (8) Abies forest (see Table 1 for descriptions). Localities of the forest types (dominant canopy trees, 11,700 unique records in total) were obtained from the third national forest resource inventory, conducted by the Taiwan Forest Bureau in 1993 (Taiwan Forest Bureau, 1995).

Table 2. All environmental variables calculated in this study. Asterisks indicating variables used in model building. Environmental variable Unit Calculation Citation (Abbreviation)

Annual mean temperature Average monthly mean 1 °C (Tmean)* temperature 2 Annual precipitation (Pannual)* Millimetre Average monthly precipitation Decimal The standard deviation of the 3 Temperature seasonality (Tsd)* fraction monthly mean temperatures (Hijmans et Decimal The coefficient of variation of the al., 2005) 4 Precipitation seasonality (Pcv)* fraction monthly mean precipitation Mean temperature of warmest 5 month The monthly mean temperature Mean temperature of coldest of the warmest or coldest month 6 month Mean temperature of wettest 7 quarter The average monthly mean °C temperature of the three wettest (Nix, 1986) Mean temperature of driest 8 or driest contiguous months quarter Mean temperature of warmest 9 The average monthly mean quarter temperature of the three Mean temperature of coldest warmest or coldest contiguous 10 quarter months

‐Table continued next page‐

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11 Precipitation of wettest month The monthly precipitation of the 12 Precipitation of driest month wettest or driest month 13 Precipitation of wettest quarter The total precipitation of the three wettest or driest Millimetre 14 Precipitation of driest quarter contiguous months Precipitation of warmest 15 The total precipitation of the quarter three warmest or coldest 16 Precipitation of coldest quarter contiguous months 17 Temperature annual range °C Variable 5 minus variable 6 Precipitation ratio of coldest Decimal Variable 17 as a percentage of 18 quarter fraction variable 2 Sum of monthly mean 19 Warmth index °C (Kira, 1977) temperature above 5 °C Monthly precipitation minus Millimetre (Lee et al., 20 Total water deficiency (Pdef)* doubled monthly mean minus °C 1997) temperature Mean annual biotemperature Potential evapotranspiration Decimal (Anderson 21 divided by total annual ratio fraction et al., 2002) precipitation P01*, P04*, P05*, P06*, P07*, 22 Monthly rainfall (P01–P12) Millimetre P10* Average terrain slopes of 1 km2 23 Inclination (slope)* Degree land area Transformed by sin(aspect rad), cos(aspect rad), and assigned Ordinal ordinals: 0: flat, 1: (–1)–(–0.75), 24 Aspect (Eastness*, Northness*) numbers: 2: (–0.75)–(–0.5), 3: (–0.5) –(– 0~8 0.25), 4: (–0.25)–0, 5: 0–0.25, 6: 0.25–0.5, 7: 0.5–0.75, 8: 0.75–1 The distance to the nearest (Lee et al., 25 (Dto3000)* Metre location above 3000 m asl 1997) No soil (0), Inceptisols (1), Oxisols Cardinal (2), Alfisols (3), Spodosols (4), (Guo et al., 26 Soil category (Soilcode)* numbers: Mollisols (5), Entisols (6), Ultisols 2005) 0~9 (7), Andisols (8), Vertisols (9)

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES

Environmental variables preparation

Present climate data were derived from an array of weather stations (data recorded from 1900 to 1990). Future projected climate data (for the years 2050, 2080 and 2100, determined by decadal average) were obtained from the Intergovernmental Panel on Climate Change (IPCC) Third Assessment Report (IPCC, 2001). By 2100, based on Taiwan regional averaging, a greater temperature increase is predicted for scenario A2 (4.8 °C) than for scenario B2 (3.2 °C), and predicted annual rainfall increases are 193 mm for A2 and 79 mm for B2. The simulated climate data were statistically downscaled to a resolution of 1 km2 to match the resolution of the present day data (35,928 grid cells in total; Wilby and Wigley, 1997, Lin et al., 2010) for the purposes of regional assessment. Based on monthly temperature and rainfall data, we calculated ecologically-relevant climate variables representing annual trends (such as mean annual temperature), seasonality (for example temperature seasonality) and extreme or limiting climatic factors (such as water deficiency) (Nix, 1986). To avoid multicollinearity (Heikkinen et al., 2006), we applied correlation tests between variables to exclude highly correlated (Pearson’s r > 0.75) factors. Along with one edaphic and four topographic factors, 16 environmental variables with low correlation were eventually selected for model building (Table 2).

Modelling species distributions and model validation

The species distributions were modelled with the maximum entropy method (MaxEnt, version 3.3.3; http://www.cs.princeton.edu/~schapire/maxent/). This programme was developed for modelling species’ geographic distributions with presence-only data, and has been shown to outperform the majority of other modelling applications, especially when sample sizes are small (Elith et al., 2006; Hijmans and Graham, 2006; Pearson et al., 2007; Graham et al., 2008; Wisz et al., 2008; Mateo et al., 2010). MaxEnt is particularly suited for epiphytes, since most epiphyte species (especially orchids) are notoriously rare, and it puts no weight on the absence of an epiphyte in a forest, which is difficult to ensure, especially for high-canopy species. MaxEnt calculates a probability distribution over the grid, which may be interpreted as an index of habitat suitability for a species (Elith et al., 2011). The programme also gives an estimate of the relative contribution of each environmental variable to the model by means of iterative calculations (in this study, 500 times). Furthermore, the relative magnitudes of environmental variables derived from one training set of data can be ‘projected’ to another set of environmental data, which enables MaxEnt to model species distribution under different climate conditions, such as future climate simulations (VanDerWal et al., 2009).

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Fig. 2 The stepwise hierarchical modelling approach used in this study. The procedure THRESHOLD removed species distributions below thresholds. The years 2050, 2080 and 2100 are target years for our models. Solid‐line arrows indicate SDM modelling; broken‐line arrows indicate SDM projection. Framed squares indicate our final SDMs. NL = needle forests: Abies, Picea, Tsuga, cypress and Pinus; BL = broad‐leaved forests: highland (BLH), midland (BLM) and lowland (BLL); ENVI VARs = environmental variables; EP = epiphyte.

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES

We applied a stepwise hierarchical modelling approach to simulate forest and epiphyte distributions under various climate change scenarios (Fig. 2). In the first step, forest distributions were modelled under present climatic conditions and subsequently projected on future scenarios (for the years 2050, 2080 and 2100). The modelled forest projections at year 2050 and 2080 were used as intermediate steps (Fig. 2), incorporating divergent persistence abilities for needle- (NL) and broad-leaved trees (BL). We randomly selected 70% of the forest occurrences for model building, and reserved the remaining 30% for model testing, calculating the area under the curve (AUC) value (Phillips et al., 2006). In the second step, we included species dispersal limitation as a factor affecting future forest distributions. Corlett (2009) pointed out that most plant species, depending on their dispersal vectors, probably have maximum dispersal distances of between 100 m and 1 km in tropical East Asia. In Taiwan, annual typhoons may promote long distance (up to 1 km) dispersal of conifer winged seeds (Engler and Guisan, 2009). After carefully reviewing earlier reports (Vittoz and Engler, 2007; Engler et al., 2009) and considering dispersal vectors, for our model we hypothesized a maximum horizontal dispersal distance of 1 km per year for each forest type. We calculated the maximum expanded range of each forest type with the age of the tree at maturity in target years (Table 1), and calibrated by average terrain inclinations (both 14° below and 22° above 1500 m asl). In step three, we included the persistence time of forests, being a measure of the time that trees can tolerate unfavourable climate conditions. We hypothesized a persistence of 20 years for broad- leaved trees (BLL, BLM and BLH) and 50 years for needle trees (Abies, cypress, Picea, Pinus and Tsuga) (Table 1). Accordingly, we modified the projected forest distributions at year 2100 by incorporating BL distributions at year 2080 and NL distributions at year 2050 (Figs 2 and 3). The persistent/extended distributions were assigned threshold values (i.e. minimum habitat suitability). In step four, the resulting eight forest distributions (eight variables), together with the 16 abiotic variables (Table 2) were used to model the distribution of 237 epiphyte species. For each species, we simulated present day conditions and then modelled projections for the year 2100 under both A2 and B2 climate change scenarios.

To validate our model, we used a null method to test the significance of the epiphyte SDMs (Raes and ter Steege, 2007). This analysis uses all presence records for model building, which is an advantage because the sample sizes of most epiphyte species were small. We created null-distributions (999 permutations) for 5–30 records 96

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(with intervals of one), 35–55 records (with intervals of five) and 60–100 records (with intervals of 10), and then applied a curve-fit through the upper limit of the 95% confidence interval AUC values (Fig. 4). We thus identified which epiphyte SDM had a significantly higher AUC value than expected by chance (p < 0.05). Species with a non-significant SDM were omitted from the analyses. Null analysis was not applied on forest SDMs because each forest type had more than a hundred occurrences.

Fig. 3 An example of a model incorporating dispersal limitation and tree persistence. The modelled distributions (year 2050 = blue, and year 2100 = red) outside dispersal ranges (grey bubbles) were removed from the result. Black dots indicate present day plant occurrence. Considering tree persistence, the tree distribution in year 2050 (blue grids) was assigned a threshold value (lowest suitability) and added to the 2100 distribution (red grids).

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES

Fig. 4 The area under the curve (AUC) values of species distribuon models (SDMs, ●) and the 95% confidence intervals. AUC values of the randomly drawn null‐models (ᇞ). Three curve fits indicated the consecutive modelling ‘features’ of MaxEnt (occurrence numbers range from 5–10, 10–15 and 15–100). The SDMs with AUC values above corresponding curves were judged to be significant in this study.

Data analysis

We calculated the number of newly appearing, remaining and disappearing epiphytes in each grid cell. The altitude of each grid cell was derived from digital terrain models (DTM). After testing for normality (Shapiro-Wilk test), pairs of means of median altitudes of the projected distributions were compared using one-way ANOVA, (SPSS, version 13.0, IBM). We described the dissimilarity between present and projected distributions using the Jaccard distance index (J’) and calculated the range turnover rate for each species. To create a species richness map, we first applied a threshold of sensitivity-specificity sum maximization (Liu et al., 2005) to convert the MaxEnt probability distribution to a predicted presence map for each species. Next, every single-species map was overlaid to produce a species richness map for epiphytes. The richness map was corrected for land-use change to eliminate species distributions in urbanized regions (assuming this remains unchanged in 2100).

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Table 3 the range changes (%) and altitudinal change (in metres) for each forest type under two climate change scenarios (scenarios A2 and B2; Ipcc, 2001), the area under curve (AUC) values for the forest models, and the top three factors sorted in descending order according to their relative contributions to each SDM. Broad‐leaved forest: lowland (BLL), midland (BLM), highland (BLH).

Forest Range change Altitudinal AUC Top three factors type (%) change (m) A2 B2 A2 B2 Abies –46 –49 217 239 0.9595 Tmean, Dto3000, Eastness Picea –77 –81 403 428 0.9606 Dto3000, Tmean, Tsd Tsuga –48 –53 250 279 0.9124 Tmean, Tsd, Dto3000 Cypress –54 –52 322 329 0.9113 Tmean, Pcv, Pdef Pinus –29 –29 130 148 0.8878 Tmean, Dto3000, Pdef BLH –44 –34 378 282 0.8428 Tmean, Pdef, Tsd BLM –20 –2 578 364 0.8091 Tmean, slope, P10 BLL –12 37 470 268 0.8406 Tmean, P10, Eastness

Results

Forest transitions

The SDM-generated forest distribution patterns agreed strongly with observed data (AUC values ranging from 0.809 to 0.967; Table 3). Although our models suggested that the total forest area would decrease by 27% and 4% (scenarios A2 and B2, respectively), most forest types exhibited larger area reductions (Table 3), with the exception of the lowland broad-leaved forest (BLL), which was projected to expand by 37% from its current extension under scenario B2. The largest projected reductions in range were for the Picea forest, which decreased by 77% in scenario A2 and 81% in scenario B2, followed by the cypress forest (–52% and –54%, respectively). Moreover, projected forest distributions indicated a general tendency to move to higher altitudes (Table 3). Picea, cypress and midland broad-leaved (BLM) forests showed more significant movement to higher altitudes than other forest types under both scenarios, whereas Pinus forests had the most stable distribution. According to the top-three factors contributing to each forest model, all forest types were sensitive to annual mean temperature (Tmean; Table 3). We also found that the factor distance to elevations above 3,000 m (Dto3000) and temperature-related factors (such as Tmean and Tsd) were relatively important for Picea forests, while cypress forest was also sensitive to moisture-related factors (such as Pdef and Pcv). 99

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES

October rainfall (P10) was a contributing factor to midland broad-leaved (BLM) forest distributions.

In addition to the shifting distribution patterns of the eight forest types, the relative extent of each forest type was also projected to change under climate change. Currently, the ratio (in terms of area occupied) of broad-leaved forests to coniferous forests is nearly 1:1. By the year 2100, our models suggest this ratio will be 1.5:1 under scenario A2 and 2:1 under scenario B2. Vegetation maps (Fig. 5) provided a visual indicator of predicted changes in forest type, notably in the north-east of Taiwan, especially under scenario A2 (Fig. 5b). Isolated Tsuga and Picea forests at the southern end of the Central Ridge (Fig. 1) were projected to disappear under both scenarios. The projections suggested a large decline and fragment of the cypress forest on the eastern side of the Central Ridge under scenario B2.

Fig. 5 The potential distributions of eight forest types under present and climate change conditions (scenario A2, B2; IPCC, 2001) in Taiwan. Since more than one forest type exists within several altitudinal zones (Abies, Picea and Tsuga >2500 m; cypress, Pinus and BLH >1500 m; BLM and BLL < 1500 m), the resulting habitat suitability of grids are compared to visually present the major forest type. Slashed boundaries indicate reserves suggested for forest monitoring. A = Chi‐Lan reserve, B = Da‐Wu reserve.

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Fig. 6 The modelled number of species lost (5a), newly appearing (5b) and remaining stable (5c) under climate change conditions (values are the average of scenarios A2 and B2, IPCC, 2001). Figure 5a indicates boundaries of present reserves in Taiwan, and suggested monitoring sites for epiphytes: (1) Chi‐Lan reserve, (2) Mt. Chia‐Li, (3) Tai‐Chi Canyon and (4) Jin‐Shuei‐Ying reserve. Occurrence of high J’ and low J' species listed in Table 4 plotted as dots in 5a and 5c, respectively.

Epiphyte transitions

After testing SDMs against null distributions, we excluded 26 non-significant SDMs (see Fig. 4). The 211 modelled epiphyte species consisted of 83 orchids, 111 ferns and 17 species belonging to other taxa (see Appendix 2). We identified the top ten most and least sensitive epiphytes to the two climate change scenarios by ranking their Jaccard distance index (J’, i.e. range turnover rate) and the three most contributing factors to the modelled distribution of each epiphyte (Table 4). Generally, relatively insensitive (low J’) species correlated with lowland forest (BLL), whilst more sensitive (high J’) species were associated with mid-elevation forests (cypress and BLM) and temperature-related factors (Tmean and Tsd). Insensitive epiphytes were generally lowland or widespread species (those with greater occurrence; see Appendix 2), whereas sensitive species were more geographically restricted (Fig. 6a, c). Under scenario A2, 83% of epiphyte species had shifted to higher altitudes by 2100; this figure was 90% for scenario B2 (see Appendix 2). In our projections, high J’ species were more likely to shift to higher altitudes than low J’ species (Table 4). The average median altitude increased by ca. 400 101

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES m under both climate change scenarios (Fig. 7). On average, 78% of epiphyte species were projected to lose 58% of their currently occupied area under scenario A2 and 77% of species were projected to lose 45% of their area under scenario B2 (see Appendix 2). Our models showed that the remainder of the species (about 20%) expanded their range size by on average 210% and 170% under scenarios A2 and B2, respectively.

At the community level, projected altitudinal shifts in epiphyte distributions brought about changing spatial patterns of epiphyte richness. At present, epiphyte diversity is highest at 1,000–1,500 m asl (nearly 100 species per 1 km2). Under climate change conditions, our model indicated that this belt of maximum species richness would shift to 1,500–2,000 m asl (Fig. 8). On average, 28 epiphytic species are projected to disappear from each grid cell under scenario A2 and 24 species under scenario B2 (Fig. 6a); the most stable species number was generally found at 1,000–1,500 m asl (Fig. 6c). Our models suggested a dramatic decrease of species richness in the north of Taiwan, which was more pronounced under scenario A2 than B2 (Fig. 8). In general, newly appearing species occurred in the southern mountains (1,500–2,000 m asl) of Taiwan (Fig. 6b).

Fig. 7 Box plot of median altitudes of 211 SDMs for present climate conditions and two scenarios of climate change (A2 and B2; IPCC, 2001). The plots present median, lower quartile, upper quartile, maximum and minimum observations. Different letters indicate significant differences (p < 0.01).

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Fig. 8 The species richness maps of epiphytes under present and climate change conditions (scenario A2, B2; IPCC, 2001). Discussion Modelled species responses and possible ecological interpretations The massive sample size of the tree occurrence data may partially contribute to the high quality of the forest models. All forest types were highly sensitive to mean annual temperature; this is expected because mean annual temperature strongly correlates with elevation, driving vegetation stratification in Taiwan (Su, 1992). Our results showed that most species, both trees and epiphytes, are projected to shift to higher altitudes. This would probably lead to increased habitat fragmentation, since landscapes are dissected by deep ravines at higher elevations. In Taiwan, Picea morrisonicola currently has a scattered distribution between 2,500 and 3,200 m asl, and our model indicates that a major factor in Picea’s distribution is distance to elevations above 3,000 m (Dto3000), producing two discrete populations separated by a depression in the middle of the Taiwan Central Ridge (Fig. 5a). Variable Dto3000 is related to Massenerhebung effect which explains the variation in altitudinal limits of forest types based on mountain sizes and locations. In Taiwan, the forest type on the main ridges of major ranges generally have higher altitudinal limits due to heat retention and wind shadowing; a phenomenon that has often been noted on small coastal islands (Grubb, 1971; Foster, 2001). The relatively small and fragmented population of Picea is thus more sensitive to global warming than the other forest types. 103

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES

Table 4 The top 10 (grey shading) and lowest 10 (white background) species for the two scenarios (A2 and B2; IPCC, 2001) sorted by their Jaccard distance index (J’), and the top three factors sorted in descending order according to their relative contributions to each SDM.

Altitudinal Altitudinal Species Scenario J' J' Factor shift (m) shift (m) A2 B2 A2 B2 Bulbophyllum chitouense* A2 1.00 0.90 496 430 Tsd, BLM, Cypress Elaphoglossum luzonicum A2, B2 1.00 0.97 –654 –160 BLM, Dto3000, soil_code Grammitis nuda* A2, B2 1.00 1.00 944 885 BLM, Dto3000, Pdef Dendrobium falconeri A2 1.00 0.82 –36 196 P10, slope, soil_code Mecodium oligosorum A2, B2 1.00 0.99 585 –162 Pdef, P01, slope Goodyera bilamellata* B2 0.97 1.00 845 530 Tmean, slope, Tsd Flickingeria tairukounia* B2 0.99 1.00 793 715 BLL, Eastness, P05 Pyrrosia matsudae* A2 1.00 0.77 383 270 P10, Dto3000, Pinus Saxiglossum angustissimum A2 1.00 0.93 661 –127 Northerness, Tsd, P10 Bulbophyllum electrinum A2, B2 1.00 1.00 –731 717 BLM, Pdef, Pinus Microtatorchis compacta A2 1.00 0.89 830 471 Tmean, BLL, Pdef Humata chrysanthemifolia A2 1.00 0.86 549 304 P05, P07, BLH Cleisostoma paniculatum B2 0.98 0.97 745 579 P10, BLH, slope Scleroglossum pusillum B2 0.95 0.96 –742 –775 Pdef, Pinus, Tsd Gastrochilus raraensis* B2 0.97 0.96 660 738 Pdef, Cypress, BLL Mecodium badium B2 0.96 0.96 1151 742 Tmean, Tsd, Pannual Psilotum nudum A2 0.73 0.61 385 197 slope, Pdef, BLL Vaginularia paradoxa A2 0.71 0.71 –54 –18 P06, BLL, BLH Davallia solida A2 0.68 0.78 –53 –128 Dto3000, Tsd, BLL Thrixspermum fantasticum A2, B2 0.66 0.47 9 56 Pdef, BLH, Pinus Vittaria taeniophylla A2, B2 0.64 0.42 –22 22 Pinus, slope, Tsuga Luisia cordata* A2, B2 0.61 0.31 12 23 soil_code, Dto3000, BLL Oberonia rosea A2, B2 0.61 0.41 24 11 Dto3000, Eastness, BLH Medinilla formosana* A2 0.55 0.59 –99 227 BLL, Dto3000, P07 Oberonia gigantea* B2 0.79 0.51 535 431 Pdef, Pinus, slope Pentapanax castanopsisicola* B2 0.84 0.51 158 243 Pdef, BLL, P05 Calymmodon cucullatus A2 0.50 0.56 –173 –61 Dto3000, P06, BLM Pomatocalpa acuminata* B2 0.84 0.48 203 135 BLH, P06, Northerness Thrixspermum formosanum B2 0.80 0.48 203 182 BLH, Eastness, Dto3000 Hoya carnosa B2 0.75 0.46 269 217 BLL, slope, BLH Schoenorchis vanoverberghii A2, B2 0.31 0.32 –3 –17 Dto3000, BLL, slope

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The model indicated a distinct decline in cypress forest, a major component of montane cloud forest in Taiwan. Cypress forest is characterized by cool temperatures, continuously moist and dim conditions, typically enveloped in clouds during the afternoon (Lai et al., 2006). Many epiphytes with restricted distributions are specialized to this particular thermal and hydrological regime. Consistent with observations, the models indicated that epiphyte distributions were strongly correlated with forest type (Table 4). Cypress forest was an important factor in the distribution of two sensitive endemic orchids (Bulbophyllum chitouense and Gastrochilus raraensis). Rainfall seasonality (Pcv) and water deficiency (Pdef) were apparently the most contributing factors to cypress forest distribution. The climate change scenarios suggest increased precipitation variability in time and space, and future weakening of the NE monsoon (Lin et al., 2010), which accounts for a substantial proportion of Taiwan’s annual rainfall, especially in the north-east. These factors are probably responsible for the projected general decline of the cypress forests and associated epiphytic species (Fig. 5b, c). October is the onset of the NE monsoon season, thus species distributions correlating closely with October rainfall (P10) are projected to have high range turnover rates (high J') under future climate conditions (Table 4).

The sensitivity of species to global climate change is often related to differences in ecological properties (Broennimann et al., 2006). Past studies suggested that generalists (i.e. species with wider niche breadths and hence larger range sizes on the environmental gradient) are expected to demonstrate broader tolerances to climate changes than specialists (Brown et al., 1995; Benzing, 1998; Thuiller et al., 2004; Broennimann et al., 2006). In other words, the species with the more critical habitat demands are probably more sensitive to climate change and may thus be suitable indicator species. Our model results confirm many sensitive (high J') epiphytes presently have restricted distributions (for example Bulbophyllum chitouense, Grammitis nuda, Flickingeria tairukounia and Saxiglossum angustissimum), whereas insensitive species (low J') are widespread, and include several pantropical species (such as Psilotum nudum or Hoya carnosa) (Table 4). Insensitive epiphytes are usually lowland species, distributed in southern Taiwan, and less sensitive to temperature-related factors (Fig. 6c and Table 4). Conversely, our results indicated temperature-related factors (Tmean and Tsd) had an important effect on the modelled distributions of sensitive epiphytes that grew in the mid-elevation/montane cloud forests (cypress, BLM and the lower altitude ranges of BLH; Fig. 6a and Table 4). Tropical montane cloud forests are unique among terrestrial ecosystems for their particular hydroregime (Still et al., 1999), and typically occur in narrow altitude belts characterized by high endemism and abundant epiphytes (Foster, 2001). Accordingly, the epiphytes specialized in this ecotone are probably thermal- or hydro-specialists. Among high J’ species, Mecodium badium is relatively widespread, yet was projected to have a high range turnover rate under climate change conditions. This filmy fern occurs widely at mid-altitudes, and its occurrence correlates 105

MODELLING CLIMATE CHANGE IMPACTS ON EPIPHYTES strongly with climate factors (i.e., annual mean temperature, Tmean; temperature seasonality, Tsd; annual rainfall, Pannual) in the distribution model; thus this species may be more susceptible to atmospheric drying in a warming climate.

In addition to climate variables, the models indicated that stable topographic or edaphic factors should be considered when modelling species distributions under climate change. Eastness was identified as an important predictor of Abies and lowland broad-leaved forest distributions (Table 3). During the NE monsoon, precipitation (in the form of snow at high altitudes) is greater on east-facing slopes than those of other aspects, exerting a significant influence on forest distributions. Austin and Van Niel (2011a) noted similar climate regime differences between north- and south- facing aspects in temperate latitudes. Soil category is a contributing factor to some epiphyte distribution models (see Appendix 2); terrestrial soil fertilities may affect nutrient availability in the canopy and hence epiphyte species compositions (Gentry and Dodson, 1987a; Benner and Vitousek, 2007). SDMs using climate- only predictors often overestimate range reduction and fail to recognize potential landscape- defined refugia when assessing climate change impacts (Austin and Van Niel, 2011b). Our study confirms terrain-related factors must be incorporated when projecting species response to climate change at a local scale.

Migration velocity

Dispersal limitation and persistence induce a lag in modelled tree displacement but forest transition may be unexpectedly rapid. Pollen records from the Andes indicated that during the last glacial maximum, the forest belt shifted by ca. 1,000 m and a massive replacement of ecotone forests occurred, implying a rapid altitudinal displacement of trees on tropical mountains (Hooghiemstra and van der Hammen, 2004; Groot et al., 2010). Clark (1998) combined field data with a population growth model to prove that plant dispersal was compatible with the rapid spread shown by paleontological records. An investigation of 13 tree species in the French mountains found that the low altitude limits of seedlings were on average 29m higher than the adult parent trees, in response to the warming trend of the past two decades (Lenoir et al., 2009). An analysis of 60,000 long-term forest inventory plots in the eastern USA suggested an approximately northward tree migration rate of 100 km per century (Woodall et al., 2009); in the Alps, the altitudinal shift may have been as much as 340 m over the past 50 years, this speed correlated with the species wind dispersal (Parolo and Rossi 2008). However, for some species and areas, establishment limits distributions more than dispersal (Alsos et al., 2007). Most epiphytes produce highly mobile propagules capable of long-distance dispersal, yet recruitment of phorophyte-dependent epiphytes inevitably lags behind the trees, particularly of those epiphytes that depend on old-growth trees for establishment. Considering the biotic interaction between epiphytes and forest trees, we used forest habitat suitability as 106

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the predictor for epiphyte modelling. This approach had the additional advantage that the range boundary of forests with low habitat suitability for trees, hence, for epiphytes, was also assessed in the model.

Conservation implications

Our model indicated a considerable decline in the area extent of mid-elevation forests and associated epiphytic species under the two climate change scenarios. Many mid-altitude species fall outside current reserves because of their proximity to aboriginal villages (Fig. 6a). We recommend establishing two long-term forest monitoring sites in the Chi-Lan and Da-Wu reserves (Fig. 5). Chi-Lan is dominated by primitive cypress and Picea forests, and is an ideal site for monitoring forest type change. In south Taiwan, Da-Wu reserve lies in a region where coniferous forests are projected to be replaced by shadier broad-leaved forests, thus favouring an increase in shade-tolerant epiphytes. We anticipate that tree and epiphyte populations will change relatively rapidly at Da-Wu. Secondly, we recommend that three mid-altitude sites be established for epiphyte monitoring, at Mt. Chia-Li, Tai-Chi Canyon and Jin-Shuei-Ying reserve (Fig. 6a). Jin-Shuei-Ying reserve is characterized by a rich diversity of epiphytic ferns and is thus an ideal site for monitoring climate-sensitive species, including two locally rare epiphytic ferns (Elaphoglossum luzonicum and Grammitis nuda; Table 4). Mt. Chia-Li and Tai-Chi Canyon are near human settlements, and currently lie outside conservation areas, but both areas are rich in epiphytic orchids and contain the majority of the local sensitive species (Table 4). Long-term plots in these locations can be used to investigate the effects of anthropogenic disturbance on sensitive epiphytes in a changing climate, thus evaluating the effectiveness of the present conservation reserves.

Global warming effects seem to be less pronounced in undisturbed forests; human disturbance may produce vacant niches for invasive species (Aptroot and van Herk, 2007). Thus, conserving old-growth forests may be crucial in supporting species to resist climate change (Ellis et al., 2009). Our climate change models showed that midlands are likely to remain richer in epiphyte species than higher or lower altitudes (Fig. 6c), thus present centres of species diversity will probably retain their importance into the future (Venter et al., 2010). On a regional scale, a mountainous island such as Taiwan may act as a potential refuge during climate change; high mountains provide the space for species migration, as most likely occurred after the Quaternary glaciations (Hsu and Wolf, 2009).

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Mt. Chia‐Li Chi‐Lan

Tai‐Chi Canyon

Da‐Wu Jin‐Shuei‐Ying

The recommended sites in Taiwan for monitoring the influence of changing climates on forests, Chi‐Lan and Da‐Wu reserves (blue boundaries) and on epiphytes, Mt. Chia‐Li, Tai‐Chi Canyon and Jin‐Shuei‐Ying (orange dots). Two sites (dashed circle) indicate areas with high epiphyte richness, HsuehShan and AliShan, located in the northern and central part of the island, respectively.

CHAPTER 8

Conclusions

Patterns in composition and distribution of vascular epiphytes

To investigate and explain regional patterns in species richness along gradients is one of the major challenges for ecological and biogeographical research. To date, few epiphyte studies are available from the Paleotropics. Moreover, most studies focus on tropical areas, whilst epiphyte research from sub-tropical areas remains scarce. In chapter 2, data is provided on the distribution of epiphyte diversity in Taiwan, a subtropical mountainous island in East Asia, to complement the perplexity of global patterns. Similar to the epiphyte flora in tropical areas, the epiphyte diversity in Taiwan was dominated by few higher taxa (families), mostly monocotyledons. Lacking several species-rich epiphyte families (e.g. Bromeliaceae and Marcgraviaceae) that have evolved independently in the Neotropics, the most abundant epiphytes in the checklist were ferns, followed by orchids. The taxonomic composition of the epiphyte flora demonstrated the transitional aspect of Taiwan, incorporating both tropical and sub-tropical regions, corroborating a trend of increasing proportion of epiphytic ferns and fern-allies with latitudes (Wolf and Flamenco-S, 2003; Zotz, 2005).

In addition to the latitudinal gradient, the presence of an extensive mountain system on the island provides an ideal opportunity for studying species richness patterns along an elevational gradient. Using 39,084 unique botanical collections, in chapter 3 the epiphyte richness was found to show a mid-elevation peak at ca. 1000 m asl. This often described phenomenon of a hump-shaped curve in species richness could not be explained by the mid- domain effect, as observed in some other studies, but coincided with the richness pattern of bryophytes on an island in the Indian Ocean (Cardelús et al., 2006; Ah-Peng et al., 2012). The epiphyte pattern in species richness showed a peak of substantially higher species richness and at slightly lower elevation than expected under the null model. The latter is presumably explained by the Massenerhebung effect (i.e. mountain mass elevation effect, Bruijnzeel et al., 1993). This phenomenon occurs on isolated, small coastal mountains, where floristically-similar vegetation types tend to be distributed at lower altitude than on large mountain masses, due to a steep lapse rate of temperature and cloud formation (Flenley, 1995).

The exceptional high species richness beyond the expectation of the null model can probably be attributed to a large number of species with a small range size, related to fine niche partitioning. For example, the restricted altitudinal band of Chamaecyparis-dominated “cypress” cloud forest (1800-2500 m) is inhabited by no less than 92 species of rare ferns (Moore 2000).

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Moreover, extraordinary endemism has been observed in the mountains and, for instance, several epiphytic orchid genera, Bulbophyllum (24 spp.), Gastrochilus (9 spp.) and Oberonia (7 spp.), show a high endemicity of nearly 50 percent. Further analysis in chapter 3 on the altitudinal ranges of species showed a higher degree of thermal specialization in the upper-zone of mountains than in the lowlands, which is in contrast to the Rapoport Effect hypothesis (Stevens, 1992). Interestingly, a transplant experiment suggested that also at the intraspecific (Asplenium antiquum) level, there was more genetic adaptation of populations at higher elevations (chapter 6). In summary, the results of above mentioned chapters suggest that environmental factors mostly account for the observed epiphyte distribution in Taiwan. In this light, the approach in chapter 7 to use species distribution models (SDMs) to assess potential range change of epiphytes under future climate conditions is reasonable.

Common features of vulnerable epiphyte species and biomes to climate change

In chapter 7, the SDMs indicated a large proportion of epiphytes that were projected to have a high range turnover rate under climate change scenarios (referred to here as “sensitive” species) presently have restricted distributions in the mountain area (e.g. Bulbophyllum chitouense, Grammitis nuda, Flickingeria tairukounia, Saxiglossum angustissimum), whereas species with a low range turnover (“insensitive”) are generally widespread lowland species, including several pantropical species (e.g. Hoya carnosa, Psilotum nudum). Corroborated by the findings of chapter 3, presumably the sensitivity and/or vulnerability of species under climate change is mostly correlated with thermal specialisation. The SDMs did indicate that temperature-related factors (Tmean and Tsd, appendix) had an important effect on the modelled distributions of sensitive epiphytes, and many of them occurred only in the mid-elevation cloud forests (e.g. cypress forest). The SDMs projected a distinct decline of cypress forest under future climates, and showed that here rainfall seasonality (Pcv) and water deficiency (Pdef) were the most contributing factors to the distribution of cypress forest. This forest is typically enveloped in clouds during the afternoon and characterized by cool temperatures and continuously moist and dim conditions (Still et al., 1999; Lai et al., 2006). Many epiphytes with restricted distributions (e.g. Bulbophyllum chitouense and Gastrochilus raraensis) are specialized to this particular thermal and hydrological regime (chapter 3). In addition, the SDM result in chapter 3 showed that species with a narrow niche-width (specialists) often have a scattered distribution. Under future warming scenarios, most species were projected to shift to higher altitudes (chapter 7), which may result in increased habitat fragmentation due to isolation of deep ravines at higher elevations. High elevation specialist species, having a relatively small range size and fragmented population, are likely most susceptible to global warming.

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In agreement with many prior studies, the ordination analysis in chapter 3 suggested that, next to light conditions, temperature and water availability were most crucial for epiphyte distribution (Gentry and Dodson, 1987a, Benzing, 1990, Wolf, 1994). In chapter 4, the experiment on Hoya carnosa indicated that even in a wet subtropical forest, water conservation was the likely ecophysiological significance of CAM instead of CO2 availability. In fact, there exists a positive correlation between air humidity and CAM/C3 species ratio (Monteiro et al., 2008). The drought-tolerance adaptation might be beneficial under future climate change of increasing seasonal variation and weather extreme. A contrasting example was represented by the filmy fern Mecodium badium. Although presently widespread, this epiphytic fern was projected to have a high range turnover rate under climate change scenarios (chapter 7). Since the fern's frond consists of only a single layer of cells, absorbing moisture from the air, this species may be particularly susceptible to atmospheric drying in a warming climate. However, many epiphytes may be more tolerant to drought stress than usual expectations. For example, the widespread and abundant population of bird's nest ferns on the island suggests their successful adaptation to the canopy environment, especially in some dry forests at the highlands. In chapter 5, an experiment to explore the physiological plasticity of Asplenium nidus revealed its flexibility in photosynthetic capacity to diverse microclimates. The experiment accidentally found that A. nidus lacked stomata on the adaxial surface of leaf blades, which likely also is a morphological adaptation to drought stress. Moreover, drought tolerance may vary amongst populations of the same species. A transplant experiment with altitudinally widespread Asplenium antiquum indicated intraspecific variation of drought tolerance (chapter 6).

Species distribution modelling: what can we learn from the MaxEnt approach?

Despite some uncertainties (Barry and Elith, 2006; Pearson et al., 2006), present studies (chapter 3 and 7) demonstrated that species distribution modelling or ecological niche modelling was a practical tool for assessing species richness patterns or evaluating the impact of climate change. Consistent with field observations, the models indicated that epiphyte distributions were strongly correlated with forest type, suggesting the importance of considering biotic interactions for modelling dependent species such as epiphytes. Moreover, SDMs confirmed that terrain-related factors (e.g. aspect, inclination) were influential when projecting species’ response to climate change at a local scale. Incorporating stable topographic or edaphic factors into models might prevent overestimating range reduction and may help to recognize potential landscape-defined refugia when assessing climate change impacts (Austin and Van Niel, 2011).

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Since the presence-only tool MaxEnt puts no weight on the absence of a species, it is particularly suitable for modelling distribution of canopy epiphytes that are often difficult to detect from the ground (Flores-Palacios and García-Franco, 2001). In addition, MaxEnt has been proved to outperform most current SDM approaches, especially when a sample size is small (Elith et al., 2006; Hernandez et al., 2006). Although a large sample size is beneficial for accurately mapping of species ranges (Feeley and Silman, 2011), most species deserving special attention in conservation are inherently rare (Pearson et al., 2007). Thus, caution should especially be taken when modelling species with relatively few collections. In addition, it is advisable that SDM’s adopt the natural boundary of the studied species, rather than an artificial one, to prevent under-prediction of range sizes (Raes, 2012). In this respect, the island biome of this study is therefore convenient for applying a SDM approach. Another particularly important decision of presence-only SDMs is how to select background samples (pseudo- absences) for parameterizing models (VanDerWal et al., 2009). This issue becomes even more relevant since more than half of the epiphyte species in this study were present with less than 50 collections. It is advised that background sample should include the full environmental range required by the species, and exclude the areas where species might not disperse to or that are unsuitable for the species (Elith et al., 2011). In chapter 3, by using a full set of data comprising unique epiphyte occurrences (29,087 out of 35,928 of the total island area) for backgrounds sampling, the model reliability was improved substantially.

MaxEnt is known to be more robust than most methods when dealing with correlated variables, thus there is less necessity to pre-select predictors for this approach (Elith et al., 2011). However, when correlated predictor variables are used, variable contributions should be interpreted with care (Phillip, 2006). In addition, it is advisable to use correlation tests or ordination analyses for pre-selection of the candidate predictors to avoid over- parameterizing models if the sample size is small, thus providing limited information on the distribution of species and their environment. The transformation of predictors in MaxEnt is termed feature, which determines model complexity. Currently, MaxEnt has six feature classes: linear, product, quadratic, hinge, threshold and categorical. The programme by default (i.e. using Auto features) restricts models to simple features if few samples were introduced (linear feature at < 10 samples, linear and quadratic at 10−14 samples, linear, quadratic and hinge at 15−79, all six features at > 79 samples). The hinge feature is recommended for substantially improving model performance (Phillips and Dudik, 2008; Elith et al., 2011), however a simple feature may be sufficient for an adequate sample as being found in chapter 3 (Syfert et al., 2013).

For a species presence-only model such as MaxEnt, it is unclear what particularly diagnostic tool should be used for model validation. It is advisable that with presence-only data multiple evaluation measures are used to determine the accuracy of the produced models

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(Hernandez et al., 2006). MaxEnt also generates the commonly used statistical area under the ROC curve (AUC) for the assessment of prediction errors in conventional presence/absence models. Yet, instead of the standard commission rate (i.e. false positive rate or fraction of true absences being predicted false present), the fraction of total predicted study area present is used in MaxEnt. Therefore, the AUC values tend to be higher for species with narrow ranges than widespread species, and a high AUC value necessarily does not suggest a better model. Consequently, in chapter 3 and 7 a null method was adopted to test the significances of the SDMs (Raes and ter Steege, 2007). A thousand random-permutation SDMs were generally performed for sample sizes of less than 100 occurrences, and those SDMs that had a significantly higher AUC value than expected by chance (p<0.05) were identified. In chapter 3, additional AIC values (Akaike’s Information Criterion) were calculated to determine whether the models had more parameters than samples, which would violate the assumptions of AIC (Warren and Seifert, 2010). Finally, it is noted that MaxEnt provides several options for repeat sampling and cross-validation, which makes it especially appropriate for small sample sizes, avoiding the use single training/test splits.

Recommendations on conservation and management of forests and associated epiphytes

The SDMs in chapter 7 projected a dramatic decline of several forests under future changing climates. To confirm this result, the establishment of two permanent forest research sites is recommended for monitoring the trend on forest composition change, for example, by recording seedling establishment and the trunk diameter growth of adult trees. The two sites, Chi-Lan (棲蘭) and Da-Wu (大武) reserves, are located in the northern and southern island at similar elevations (ca. 1500-2000 m asl), yet comprising distinct tree species due to regional climate dissimilarity (Fig. 1). The Chi-Lan site is a primary forest, dominated by old-growth cypress and Picea trees, receiving substantial influence from NE monsoon. The future climate change scenario projects weakening of the NE monsoon, and consequently a substantial decrease in annual rainfall of this area, which might account for the prediction of major decline for the local forests (Lin et al., 2010). Accordingly, Chi-Lan may provide the first-order information on the climate change impacts on forests in the relatively near future. Despite sharing a common feature of cloud forests with Chi-Lan, the Da-Wu site mainly comprises broad-leaved trees (e.g. Fagaceae) due to less influence from NE monsoon and its relatively southern latitude. Here the common coniferous tree Tsuga chinensis var. formosana was projected to be replaced by broad-leaved forests which might in turn favour shade-tolerant epiphytic species. Since broad-leaved trees and associated epiphytes are characterized by a shorter generation time than coniferous trees, the Da-Wu site is a promising site for observing climate change influence in a relatively short period of time.

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The SDMs of chapter 3 identified two areas, HsuehShan (雪山) and AliShan (阿里山), with high epiphyte diversity and endemism that deserve special attention in conservation (title figure). Receiving adequate precipitation from SW flows, these two epiphyte hotspots harbour many epiphytic orchids. It was reported recently that terrestrial species in the Alishan area showed an upward-shift of ca. 3.6 m yr-1 in their range by comparing recorded upper range limits in 1906 with those of 2006 (Jump et al., 2012). However, no study concerning the dynamic of abundant epiphyte populations here is known to date. In chapter 7, many sensitive species that are projected to have a high range-turnover rate under climate change also occurred in these two areas. Considering present species diversity and the severity of anthropogenic disturbance (e.g. climate change, land-use change), three sites (title figure), Mt. Chia-Li (棲蘭山), Tai-Chi Canyon (太極峽谷) and Jin-Shuei-Ying (浸水營), are prioritized for epiphyte conservation, requiring in-depth investigations. The former two sites, Mt. Chia-Li (ca. 1000-2000 m asl) and Tai-Chi Canyon (ca. 1000 asl), are located in HsuehShan and AliShan respectively. Both sites are near human settlements and currently lie outside conservation areas. Consequently, both sites are prone to species extinction. Several rare epiphytic orchids here (e.g. Bulbophyllum rubrolabellum, Bulbophyllum tokioi, Cymbidium floribundum, Dendrobium falconeri, Eria javanica, Gastrochilus ciliaris, Gastrochilus fuscopunctatus, Gastrochilus raraensis, Thelasis pygmaea, Pleione bulbocodioides, Thrixspermum pensile) are potential indicators for monitoring anthropogenic influences, including climate change. The last site, Jin-Shuei-Ying (ca. 500−1500 m asl) is located in the very south of Taiwan, characterized by a primary tropical montane cloud forest and an high endemism in epiphytic ferns (e.g. Grammitis nuda, Crepidomanes palmifolium). Many epiphytic ferns here are notorious rare and particularly hydro-sensitive (e.g. Hymenophyllaceae, Grammitidaceae), thus Jin-Shuei-Ying is an ideal site for monitoring climate change influence on water regime (e.g cloud formation) and population dynamics of climate-sensitive epiphytes.

Global warming effects seem to be less pronounced in undisturbed forests, and present centres of species diversity might retain their importance into the future (Aptroot and van Herk, 2007; Venter et al., 2010). Thus, conserving old-growth forests as in above mentioned sites is crucial in supporting species to resist climate change, particularly those epiphytes that depend on old-growth trees for establishment (Ellis et al., 2009). SDMs showed that mid-elevation forests will remain relatively rich in epiphyte species, yet become more fragmented under future climate change (chapter 7). The combination of anthropogenic habitat disturbance and destruction, over-collection, and the ongoing climate change will likely increase the risk for extinction, particularly for mid-elevational tree species and their associated epiphytes. The present study on the ecology and distribution of epiphytes provides a framework for future conservation strategies and highlights the urgency of conservation actions under global climate change. Future conservation strategies should enable conservation authorities to evaluate the effectiveness of conservation and management efforts.

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Appendix 1 The vascular epiphyte checklist of Taiwan

(Abbreviations: E: Epiphyte, FacuE: Facultative epiphyte, HemiE-P: Primary hemi-epiphytes, HemiE-S: Secondary hemi-epiphyte, EndemicF: endemic species in Taiwan, EndemicL: endemic species in Lanyu, EndemicG: endemic species in Lutao, floristic codes refer to Fig. 2 in Chapter2). no Family Species/ taxon Habit Floristic_Region Pteridophytes 1 Aspleniaceae Asplenium adiantoides FacuE 15, 18, 22, 29 2 Aspleniaceae Asplenium antiquum E 2 3 Aspleniaceae Asplenium australasicum E 18, 22, 29 4 Aspleniaceae Asplenium bullatum E 16, 17 5 Aspleniaceae Asplenium cuneatiforme E EndemicF 6 Aspleniaceae Asplenium ensiforme FacuE 2‐25, 17, 16 7 Aspleniaceae Asplenium griffithianum FacuE 2‐20, 16, 17 8 Aspleniaceae Asplenium incisum FacuE 2 9 Aspleniaceae Asplenium laciniatum E 2‐27 10 Aspleniaceae Asplenium neolaserpitiifolium E 2‐20, 17 11 Aspleniaceae E 2‐20, 17, 18, 19, 20, 21, 22, 23, Asplenium nidus 29, 15, 12 12 Aspleniaceae Asplenium normale FacuE 2, 15, 17, 18, 20, 29, 12, 21 13 Aspleniaceae Asplenium oldhami FacuE 2‐20, 17 14 Aspleniaceae Asplenium planicaule FacuE 2, 17, 18‐104 15 Aspleniaceae Asplenium prolongatum FacuE 16, 17, 2 16 Aspleniaceae Asplenium pseudolaserpitiifolium E 17 17 Aspleniaceae Asplenium ritoense FacuE 2, 17 18 Davalliaceae Araiostegia parvipinnata E 2‐25 19 Davalliaceae Davallia formosana E 17 20 Davalliaceae Davallia mariesii E 2 21 Davalliaceae Davallia solida E 17, 18, 22 22 Davalliaceae Humata chrysanthemifolia E 18‐104 23 Davalliaceae Humata griffithiana E 2‐27, 2‐25 24 Davalliaceae Humata pectinata E 18, 20, 29 25 Davalliaceae Humata repens E 2, 15, 17, 18, 29 26 Davalliaceae Humata trifoliata E 2‐20, 17, 18 27 Davalliaceae Humata vestita E 17, 18 ‐CONTINUED‐

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28 Davalliaceae Leucostegia immersa E 2‐27, 16, 17, 18 29 Grammitidaceae Calymmodon cucullatus E 16, 18, 22, 29 30 Grammitidaceae Calymmodon gracilis E 17, 18 31 Grammitidaceae Ctenopteris curtisii E 18 32 Grammitidaceae Ctenopteris merrittii E 18 33 Grammitidaceae Ctenopteris mollicoma E 18 34 Grammitidaceae Ctenopteris obliquata E 16, 17, 18 35 Grammitidaceae Ctenopteris subfalcata E 16, 17, 18 36 Grammitidaceae Ctenopteris tenuisecta E 18 37 Grammitidaceae Grammitis adspera E 18, 29 38 Grammitidaceae Grammitis congener E 17, 18 39 Grammitidaceae Grammitis fenicis E 18‐104 40 Grammitidaceae Grammitis intromissa E 18 41 Grammitidaceae Grammitis jagoriana E 18 42 Grammitidaceae Grammitis nuda E EndemicF 43 Grammitidaceae Grammitis reinwardtia E 18 44 Grammitidaceae Prosaptia contigua E 16, 18, 19, 20, 22, 29 45 Grammitidaceae Prosaptia urceolaris E 17, 18 46 Grammitidaceae Scleroglossum pusillum E 17, 18 47 Grammitidaceae Xiphopteris okuboi E 2, 17 48 Hymenophyllaceae Abrodictyum cumingii E 2, 18 49 Hymenophyllaceae Crepidomanes bilabiatum E 2‐20, 17, 18 50 Hymenophyllaceae Crepidomanes birmanicum E 2, 17, 16 51 Hymenophyllaceae Crepidomanes kurzii E 16, 17, 18, 29 52 Hymenophyllaceae Crepidomanes latealatum FacuE 2, 16, 17, 18 53 Hymenophyllaceae Crepidomanes latemarginale FacuE 2‐20, 16, 17, 18 54 Hymenophyllaceae Crepidomanes palmifolium E EndemicF 55 Hymenophyllaceae Crepidomanes schmidtianum var. FacuE 2‐27, 18‐104 latifrons 56 Hymenophyllaceae Gonocormus minutus E 2, 16, 17, 18, 20, 22 57 Hymenophyllaceae Hymenophyllum barbatum E 2, 16, 17 58 Hymenophyllaceae Hymenophyllum devolii E EndemicF 59 Hymenophyllaceae Hymenophyllum fimbriatum E 18‐104 60 Hymenophyllaceae Hymenophyllum productum E 17, 18 61 Hymenophyllaceae Hymenophyllum simonsianum E 2‐27 62 Hymenophyllaceae Hymenophyllum taiwanense E EndemicF 63 Hymenophyllaceae Mecodium badium E 2, 16, 17, 18 ‐CONTINUED‐

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64 Hymenophyllaceae Mecodium javanicum E 16, 18, 19 65 Hymenophyllaceae Mecodium oligosorum E 2 66 Hymenophyllaceae Mecodium polyanthos E 2, 15, 17, 18 67 Hymenophyllaceae Mecodium wrightii E 2, 4 68 Hymenophyllaceae Meringium blandum E 18 69 Hymenophyllaceae Meringium denticulatum FacuE 2‐20, 16, 17, 18, 19 70 Hymenophyllaceae Meringium holochilum FacuE 18 71 Hymenophyllaceae Microgonium bimarginatum FacuE 2‐20, 16, 17, 18, 20, 29 72 Hymenophyllaceae Microgonium motleyi FacuE 2‐20, 16, 17, 18, 20 73 Hymenophyllaceae Microgonium omphalodes FacuE 2‐20, 18, 20, 29 74 Hymenophyllaceae Microtrichomanes nitidulum E 16, 17, 18, 29 75 Hymenophyllaceae Pleuromanes pallidum E 16, 17, 18, 20 76 Hymenophyllaceae Vandenboschia auriculata E 2, 16, 17, 18, 20 77 Hymenophyllaceae Vandenboschia maxima FacuE 2‐20, 17, 18 78 Hymenophyllaceae E 2‐27, 2‐20, 6, 12, 16, 17, 18, 23, Vandenboschia radicans 24, 25, 27 79 Lomariopsidaceae Elaphoglossum callifolium E 17, 18 80 Lomariopsidaceae Elaphoglossum commutatum E 10, 12, 15, 16, 18, 21, 25 81 Lomariopsidaceae Elaphoglossum luzonicum E 18 82 Lomariopsidaceae Elaphoglossum marginatum E EndemicF 83 Lomariopsidaceae Elaphoglossum yoshinagae E 2, 17 84 Lomariopsidaceae Lomariopsis spectabilis E 2‐20, 18 85 Lycopodiaceae Lycopodium carinatum E 2‐20, 17, 18, 20, 29 86 Lycopodiaceae Lycopodium cryptomerianum E 2 87 Lycopodiaceae Lycopodium cunninghamioides E 2 88 Lycopodiaceae Lycopodium fargesii E 2 89 Lycopodiaceae Lycopodium fordii E 2, 16, 17 90 Lycopodiaceae Lycopodium phlegmaria E 2, 18, 22, 29, 15, 12 91 Lycopodiaceae Lycopodium salvinioides E 2‐20, 18‐104 92 Lycopodiaceae Lycopodium sieboldii E 2 93 Lycopodiaceae Lycopodium squarrosum E 2, 20, 18, 22 94 Lycopodiaceae Lycopodium taiwanense E 2‐27, 2‐20, 16 95 Oleandraceae FacuE 2‐20, 16, 17, 18, 9, 23, 24, 25, Nephrolepis auriculata 26, 27, 22, 21, 15, 29 96 Oleandraceae FacuE 2‐20, 19, 20, 18, 23, 12, 15, 16, Nephrolepis biserrata 10, 29, 27, 25 97 Oleandraceae Nephrolepis multiflora FacuE 2‐20, 16, 17, 18‐104 ‐CONTINUED‐

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98 Oleandraceae Oleandra wallichii E 2‐25, 2‐27, 16, 17 99 Opioglossaceae Ophioderma pendula E 17, 18, 15, 21, 29 100 Polypodiaceae Aglaomorpha meyeniana E 18‐104 101 Polypodiaceae Arthromeris lehmanni E 2, 16, 17, 18‐104 102 Polypodiaceae Belvisia mucronata E 16, 18, 20, 22, 19, 29 103 Polypodiaceae Colysis hemionitidea FacuE 2‐27, 16, 17, 18‐104 104 Polypodiaceae Colysis pothifolia FacuE 2, 16, 17, 18‐104 105 Polypodiaceae Colysis shintenensis FacuE 2 106 Polypodiaceae Colysis wrightii FacuE 2‐20, 17 107 Polypodiaceae Crypsinus echinosporus E EndemicF 108 Polypodiaceae Crypsinus engleri E 2 109 Polypodiaceae Crypsinus hastatus FacuE 2, 18‐104 110 Polypodiaceae Crypsinus quasidivaricatus FacuE 2‐27, 16 111 Polypodiaceae Crypsinus taeniatus var. FacuE 18, 20 palmatus 112 Polypodiaceae Crypsinus taiwanensis FacuE EndemicF 113 Polypodiaceae Crypsinus yakushimensis FacuE 2‐20 114 Polypodiaceae Drymotaenium miyoshianum E 2 115 Polypodiaceae Drynaria fortunei E 17 116 Polypodiaceae Lemmaphyllum diversum E 2 117 Polypodiaceae Lemmaphyllum microphyllum E 2 118 Polypodiaceae Lepisorus clathratus E 2, 8, 16 119 Polypodiaceae Lepisorus kawakamii E EndemicF 120 Polypodiaceae Lepisorus kuchenensis E 2‐25 121 Polypodiaceae Lepisorus megasorus E EndemicF 122 Polypodiaceae Lepisorus monilisorus E EndemicF 123 Polypodiaceae Lepisorus morrisonensis E 2‐25, 2‐27 124 Polypodiaceae Lepisorus obscurevenulosus E 2 125 Polypodiaceae Lepisorus pseudoussuriensis E EndemicF 126 Polypodiaceae Lepisorus suboligolepidus E 2 127 Polypodiaceae Lepisorus thunbergianus E 2, 18‐104 128 Polypodiaceae Lepisorus tosaensis E 2 129 Polypodiaceae Leptochilus decurrens FacuE 16, 17, 18, 20 130 Polypodiaceae Loxogramme confertifolia E EndemicF 131 Polypodiaceae Loxogramme formosana E 2‐25 132 Polypodiaceae Loxogramme grammitoides E 2 133 Polypodiaceae Loxogramme remotefrondigera E EndemicF ‐CONTINUED‐

142

APPENDIX 1

134 Polypodiaceae Loxogramme salicifolia E 2, 17 135 Polypodiaceae Microsorium buergerianum E 2, 17 136 Polypodiaceae Microsorium dilatatum E 2‐20, 16, 17 137 Polypodiaceae Microsorium fortunei FacuE 2‐27, 2‐20 138 Polypodiaceae Microsorium membranaceum FacuE 2‐25, 2‐27, 16, 17, 18‐104 139 Polypodiaceae Microsorium punctatum E 16, 17, 22, 29 140 Polypodiaceae Microsorium rubidum E 2‐20, 16, 17, 18, 20 141 Polypodiaceae Polypodium amoenum E 2‐27, 17 142 Polypodiaceae Polypodium argutum E 2‐25, 2‐27, 17, 18‐104 143 Polypodiaceae Polypodium formosanum E 2‐20 144 Polypodiaceae Polypodium microrhizoma E 2‐25, 2‐27 145 Polypodiaceae Polypodium raishanense E EndemicF 146 Polypodiaceae Polypodium transpianense E EndemicF 147 Polypodiaceae Pseudodrynaria coronans E 2‐20, 2‐25, 2‐27, 17 148 Polypodiaceae Pyrrosia adnascens E 2‐20, 16, 17, 18, 20 149 Polypodiaceae Pyrrosia gralla E 2‐25 150 Polypodiaceae Pyrrosia linearifolia E 2 151 Polypodiaceae Pyrrosia lingua E 2, 17 152 Polypodiaceae Pyrrosia matsudae E EndemicF 153 Polypodiaceae Pyrrosia polydactylis E EndemicF 154 Polypodiaceae Pyrrosia sheareri E 17 155 Polypodiaceae Pyrrosia transmorrisonensis E EndemicF 156 Polypodiaceae Saxiglossum angustissimum E 2 157 Psilotaceae E 2, 17, 18, 21, 22, 29, 10, 12, 15, Psilotum nudum 23, 9, 3, 25, 27, 26 158 Selaginellaceae Selaginella delicatula E 2, 16, 17, 18, 20 159 Selaginellaceae Selaginella involvens E 2, 16, 17, 18 160 Selaginellaceae Selaginella stauntoniana FacuE 2 161 Selaginellaceae Selaginella tamariscina FacuE 2, 16, 18 162 Vittariaceae Antrophyum formosanum FacuE 2‐20 163 Vittariaceae Antrophyum obovatum FacuE 2, 16, 17 164 Vittariaceae Antrophyum parvulum FacuE 2‐20, 18 165 Vittariaceae Antrophyum sessilifolium FacuE 18‐104 166 Vittariaceae Vaginularia paradoxa E 16, 18, 20, 21 167 Vittariaceae Vaginularia trichoidea E 18, 21 168 Vittariaceae Vittaria anguste‐elongata E 18 169 Vittariaceae Vittaria flexuosa E 2, 16, 17, 18 ‐CONTINUED‐

143

APPENDIX 1

170 Vittariaceae Vittaria taeniophylla E 2‐27, 2‐25, 17, 18‐104 171 Vittariaceae Vittaria zosterifolia E 2‐20, 18, 20 Dicotyledons 172 Araliaceae Schefflera arboricola E 17 173 Asclepiadaceae Dischidia formosana E EndemicF&L 174 Asclepiadaceae Hoya carnosa E 2, 16, 17 175 Ericaceae Rhododendron kawakamii E EndemicF 176 Ericaceae Vaccinium dunalianum var. E EndemicF caudatifolium 177 Ericaceae Vaccinium emarginatum E EndemicF 178 Gesneriaceae Aeschynanthus acuminatus E 2‐27, 16, 17, 18 179 Gesneriaceae Lysionotus pauciflorus E 2 180 Gesneriaceae Lysionotus pauciflorus var. E EndemicL ikedae 181 Melastomataceae Medinilla formosana E EndemicF 182 Melastomataceae Medinilla hayataina E EndemicL 183 Melastomataceae Pachycentria formosana E EndemicF 184 Moraceae Ficus benjamina HemiE‐P 17, 18, 29 185 Moraceae Ficus caulocarpa HemiE‐P 2‐20, 17, 18, 16 186 Moraceae Ficus heteropleura HemiE‐P 2‐27, 18, 17 187 Moraceae Ficus microcarpa var. microcarpa HemiE‐P 2‐20, 18, 17, 16, 29 188 Moraceae Ficus microcarpa var. crassifolia HemiE‐P 18‐104 189 Moraceae Ficus pumila HemiE‐S 2, 16 190 Moraceae Ficus pumila L. var. awkeotsang HemiE‐S EndemicF 191 Moraceae Ficus sarmentosa var. henryi HemiE‐S 2 192 Moraceae Ficus sarmentosa var. nipponica HemiE‐S 2 193 Moraceae Ficus superba var. japonica HemiE‐P 2, 16, 17, 18 194 Moraceae Ficus virgata HemiE‐P 2‐20, 16, 17, 18, 29, 22 195 Piperaceae Peperomia japonica E 2 196 Piperaceae Peperomia nakaharai E EndemicF 197 Piperaceae E 2, 23, 26, 25, 21, 12, 10, 15, 25, Peperomia reflexa 29 198 Piperaceae Peperomia rubrivenosa E 18‐104 199 Piperaceae Peperomia sui E EndemicF 200 Piperaceae Piper arborescens HemiE‐S 18 201 Piperaceae Piper betle HemiE‐S 18 202 Piperaceae Piper interruptum var. HemiE‐S 18 multinervum ‐CONTINUED‐ 144

APPENDIX 1

203 Piperaceae Piper kadsura HemiE‐S 2 204 Piperaceae Piper kawakamii HemiE‐S EndemicF 205 Piperaceae Piper kwashoense HemiE‐S EndemicL&G 206 Piperaceae Piper sintenense HemiE‐S EndemicF 207 Piperaceae Piper taiwanense HemiE‐S EndemicF 208 Rubiaceae Psychotria serpens HemiE‐S 2, 17 209 Saxifragaceae Hydrangea integrifolia E 18‐104 210 Saxifragaceae Pileostegia viburnoides E 2‐20, 16, 17 211 Urticaceae Procris laevigata E 2‐25, 15, 16, 17, 18 Monocotyledons 212 Araceae Epipremnum formosanum HemiE‐S EndemicF 213 Araceae Epipremnum pinnatum HemiE‐S 2, 18, 20, 29 214 Araceae Pothoidium lobbianum HemiE‐S 18 215 Araceae Pothos chinensis HemiE‐S 2 216 Araceae E 2‐25, 15, 16, 17, 18, 12, 29, 10, Remusatia vivipara 25 217 Orchidaceae Acampe rigida E 2‐27, 16, 17, 18 218 Orchidaceae Appendicula fenixii E EndemicL 219 Orchidaceae Appendicula reflexa E 17, 18 220 Orchidaceae Arachnis labrosa E 17 221 Orchidaceae Ascocentrum pumilum E EndemicF 222 Orchidaceae Bulbophyllum affine E 2‐27, 16, 17 223 Orchidaceae Bulbophyllum albociliatum E EndemicF 224 Orchidaceae Bulbophyllum aureolabellum E EndemicF 225 Orchidaceae Bulbophyllum chitouense E EndemicF 226 Orchidaceae Bulbophyllum drymoglossum E 2 227 Orchidaceae Bulbophyllum electrinum E 2‐25, 17 228 Orchidaceae Bulbophyllum hirundinis E 17 229 Orchidaceae Bulbophyllum insulsum E 17 230 Orchidaceae Bulbophyllum japonicum E 2 231 Orchidaceae Bulbophyllum macraei E 2, 16 232 Orchidaceae Bulbophyllum melanoglossum E EndemicF 233 Orchidaceae Bulbophyllum omerandrum E 2 234 Orchidaceae Bulbophyllum pectenveneris E 17 235 Orchidaceae Bulbophyllum pectinatum E 17 236 Orchidaceae Bulbophyllum pingtungense E EndemicF 237 Orchidaceae Bulbophyllum retusiusculum E 2‐27, 17, 16 ‐CONTINUED‐

145

APPENDIX 1

238 Orchidaceae Bulbophyllum riyanum E 17 239 Orchidaceae Bulbophyllum rubrolabellum E EndemicF 240 Orchidaceae Bulbophyllum setaceum E EndemicF 241 Orchidaceae Bulbophyllum taitungianum E EndemicF 242 Orchidaceae Bulbophyllum taiwanense E EndemicF 243 Orchidaceae Bulbophyllum tokioi E EndemicF 244 Orchidaceae Bulbophyllum umbellatum E 2‐27, 16, 17 245 Orchidaceae Bulbophyllum wightii E 16 246 Orchidaceae Chiloschista segawai E EndemicF 247 Orchidaceae Cleisostoma paniculatum E 17 248 Orchidaceae Cleisostoma uraiensis E 2‐20, 18‐104 249 Orchidaceae Cymbidium dayanum E 2, 16, 17, 18 250 Orchidaceae Dendrobium catenatum E 2 251 Orchidaceae Dendrobium chameleon E 18‐104 252 Orchidaceae Dendrobium chryseum E 2, 16, 17 253 Orchidaceae Dendrobium crumenatum E 16, 17, 18 254 Orchidaceae Dendrobium equitans E 18‐104 255 Orchidaceae Dendrobium falconeri E 2‐27, 16, 17 256 Orchidaceae Dendrobium furcatopedicellatum E EndemicF 257 Orchidaceae Dendrobium goldschmidtianum E 18‐104 258 Orchidaceae Dendrobium leptocladum E EndemicF 259 Orchidaceae Dendrobium linawianum E 2 260 Orchidaceae Dendrobium moniliforme E 2 261 Orchidaceae Dendrobium somae E EndemicF 262 Orchidaceae Dendrochilum uncatum E 18‐104 263 Orchidaceae Diploprora championii E 2‐27, 16, 17 264 Orchidaceae Epigeneium fargesii E 2‐27, 17 265 Orchidaceae Epigeneium nakaharae E EndemicF 266 Orchidaceae Eria amica E 2‐25, 2‐27, 17 267 Orchidaceae Eria corneri E 2‐20, 17 268 Orchidaceae Eria japonica E 2‐20, 17 269 Orchidaceae Eria javanica E 2, 16, 17, 18 270 Orchidaceae Eria ovata E 2‐20, 18 271 Orchidaceae Eria robusta E 18 272 Orchidaceae Eria tomentosiflora E 18‐104 273 Orchidaceae Flickingeria comata E 18, 29, 19, 20, 22 274 Orchidaceae Flickingeria tairukounia E EndemicF ‐CONTINUED‐

146

APPENDIX 1

275 Orchidaceae Gastrochilus ciliaris E 2 276 Orchidaceae Gastrochilus formosanus E 2 277 Orchidaceae Gastrochilus fuscopunctatus E EndemicF 278 Orchidaceae Gastrochilus hoii E EndemicF 279 Orchidaceae Gastrochilus japonicus E 2 280 Orchidaceae Gastrochilus linii E EndemicF 281 Orchidaceae Gastrochilus matsudai E EndemicF 282 Orchidaceae Gastrochilus rantabunensis E 2 283 Orchidaceae Gastrochilus raraensis E EndemicF 284 Orchidaceae Goodyera bilamellata E EndemicF 285 Orchidaceae Goodyera pendula E 2 286 Orchidaceae Goodyera nantoensis E EndemicF 287 Orchidaceae Haraella retrocalla E EndemicF 288 Orchidaceae Holcoglossum quasipinifolium E 2 289 Orchidaceae Liparis bootanensis E 2, 17, 18 290 Orchidaceae Liparis caespitosa E 17, 18, 16, 12, 15, 19, 20 291 Orchidaceae Liparis condylobulbon E 17, 18 292 Orchidaceae Liparis cordifolia FacuE 2‐27, 2‐25, 16 293 Orchidaceae Liparis elliptica E 2, 16, 17 294 Orchidaceae Liparis grossa E 17, 18‐104 295 Orchidaceae Liparis nakaharai E EndemicF 296 Orchidaceae Liparis somai E EndemicF 297 Orchidaceae Liparis viridiflora E 2‐27, 16, 17, 18 298 Orchidaceae Luisia cordata E EndemicF 299 Orchidaceae Luisia megasepala E EndemicF 300 Orchidaceae Luisia teres E 2 301 Orchidaceae Microtatorchis compacta E 18‐104 302 Orchidaceae Oberonia arisanensis E 2‐20 303 Orchidaceae Oberonia caulescens E 2‐25, 2‐27, 17 304 Orchidaceae Oberonia gigantea E EndemicF 305 Orchidaceae Oberonia japonica E 2 306 Orchidaceae Oberonia pumila E EndemicF 307 Orchidaceae Oberonia rosea E 17 308 Orchidaceae Oberonia seidenfadenii E EndemicF 309 Orchidaceae Papilionanthe taiwaniana E EndemicF 310 Orchidaceae Phalaenopsis aphrodite E 18‐104 311 Orchidaceae Phalaenopsis equestris E 18‐104 ‐CONTINUED‐

147

APPENDIX 1

312 Orchidaceae Pholidota cantonensis E 17 313 Orchidaceae Phreatia caulescens E 18‐104 314 Orchidaceae Phreatia formosana E 2‐25, 17 315 Orchidaceae Phreatia morii E EndemicF 316 Orchidaceae Phreatia taiwaniana E EndemicF 317 Orchidaceae Pleione bulbocodioides FacuE 2 318 Orchidaceae Pomatocalpa acuminata E EndemicF 319 Orchidaceae Schoenorchis vanoverberghii E 18‐104 320 Orchidaceae Staurochilus luchuensis E 2‐20 321 Orchidaceae Sunipia andersonii E 2‐27, 16, 17 322 Orchidaceae Taeniophyllum complanatum E EndemicF 323 Orchidaceae Taeniophyllum glandulosum E 2, 17, 18, 29 324 Orchidaceae Thelasis pygmaea E 2‐27, 16, 17, 18 325 Orchidaceae Thrixspermum annamense E 17 326 Orchidaceae Thrixspermum eximium E 18‐104 327 Orchidaceae Thrixspermum fantasticum E 2‐20, 18‐104 328 Orchidaceae Thrixspermum formosanum E 17 329 Orchidaceae Thrixspermum laurisilvaticum E 2 330 Orchidaceae Thrixspermum merguense E 17, 18 331 Orchidaceae Thrixspermum pensile E 17, 18 332 Orchidaceae Thrixspermum saruwatarii E EndemicF 333 Orchidaceae Thrixspermum subulatum E 17, 18 334 Orchidaceae Trichoglottis rosea E 18‐104 335 Orchidaceae Tuberolabium kotoense E EndemicL 336 Orchidaceae Vanda lamellata E 2‐20, 18‐104

148

Appendix 2. The epiphyte species with significant SDMs (211 spp.) and their predicted changes in median altitude and area under two climate change scenarios (A2 and B2; IPCC, 2001). Stars indicate species endemic to Taiwan. Samples denotes the number of occurrences used in MaxEnt, J’ = Jaccard distance index, AUC = area under the curve value, and Dico = Dicotyledons. Bold type numbers indicate species were projected to shift downward of median altitudes or to expand range sizes.

Altitude Altitude Area Area No. Species Samples J' J' shift shift change change AUC Taxa (m) (m) (%) (%) A2 B2 A2 B2 A2 B2 1 Acampe rigida 14 0.90 0.66 374 259 ‐33 5 0.9611 Orchid Aeschynanthus 2 343 0.90 0.80 656 545 ‐51 ‐44 0.8920 Dico acuminatus Aglaomorpha 3 15 0.85 0.59 18 7 341 118 0.9802 Fern meyeniana 4 Appendicula reflexa 6 0.83 0.71 503 263 134 108 0.9968 Orchid Araiostegia 5 34 0.99 0.71 505 484 ‐86 ‐46 0.9672 Fern parvipinnata 6 Arthromeris lehmanni 182 0.87 0.74 282 370 ‐11 ‐30 0.9278 Fern Ascocentrum 7 43 0.96 0.55 416 ‐65 ‐92 ‐3 0.9327 Orchid pumilum* 8 Asplenium antiquum 642 0.79 0.58 ‐158 ‐138 99 30 0.8306 Fern Asplenium 9 129 0.76 0.55 287 140 95 101 0.9550 Fern australasicum 10 Asplenium bullatum 26 0.95 0.63 661 447 ‐57 18 0.9580 Fern Asplenium 11 180 0.96 0.90 826 643 ‐75 ‐70 0.9338 Fern cuneatiforme* 12 Asplenium laciniatum 83 0.99 0.76 560 358 ‐92 ‐39 0.9578 Fern Asplenium 13 215 0.86 0.71 447 432 54 17 0.9160 Fern neolaserpitiifolium 14 Belvisia mucronata 7 0.99 0.87 667 584 ‐73 ‐44 0.9935 Fern Bulbophyllum 15 16 0.92 0.74 394 349 ‐67 ‐60 0.9745 Orchid albociliatum* Bulbophyllum 16 12 0.76 0.60 ‐78 ‐121 ‐40 ‐35 0.9158 Orchid aureolabellum* Bulbophyllum 17 5 1.00 0.90 496 430 ‐53 256 0.9942 Orchid chitouense* Bulbophyllum 18 26 0.96 0.83 779 658 ‐92 ‐69 0.9074 Orchid drymoglossum -CONTINUED-

149

APPENDIX 2

Bulbophyllum 19 6 1.00 1.00 ‐731 717 ‐96 ‐99 0.9619 Orchid electrinum Bulbophyllum 20 12 0.97 0.88 860 738 ‐86 ‐60 0.9449 Orchid hirundinis Bulbophyllum 21 7 0.94 0.84 252 574 ‐76 ‐66 0.9411 Orchid insulsum Bulbophyllum 22 23 0.93 0.85 682 433 ‐74 ‐74 0.9377 Orchid japonicum Bulbophyllum 23 31 0.90 0.80 671 457 17 ‐8 0.9458 Orchid macraei Bulbophyllum 24 53 0.80 0.74 424 426 117 ‐9 0.9453 Orchid melanoglossum* Bulbophyllum 25 17 0.99 0.74 716 483 ‐96 ‐53 0.9713 Orchid pectenveneris Bulbophyllum 26 31 0.78 0.55 393 350 ‐15 ‐2 0.9304 Orchid pectinatum Bulbophyllum 27 64 0.89 0.77 720 643 3 5 0.9082 Orchid retusiusculum Bulbophyllum 28 15 0.89 0.71 317 454 ‐47 ‐37 0.9664 Orchid setaceum* Bulbophyllum 29 5 0.82 0.74 20 ‐106 164 60 0.9824 Orchid taiwanense* 30 Bulbophyllum tokioi* 15 0.95 0.63 445 376 ‐71 7 0.9437 Orchid Calymmodon 31 7 0.50 0.56 ‐173 ‐61 ‐22 ‐19 0.9885 Fern cucullatus 32 Calymmodon gracilis 11 0.95 0.91 992 935 ‐87 ‐73 0.9605 Fern 33 Chiloschista segawai* 11 0.97 0.53 249 218 ‐75 ‐43 0.9548 Orchid Cleisostoma 34 38 0.98 0.97 745 579 ‐3 ‐85 0.9429 Orchid paniculatum Crepidomanes 35 107 0.98 0.88 879 800 ‐83 ‐60 0.9401 Fern birmanicum Crepidomanes 36 12 0.95 0.65 ‐86 391 ‐72 18 0.9486 Fern palmifolium* Crypsinus 37 60 0.92 0.93 547 749 ‐71 ‐88 0.9444 Fern echinosporus* 38 Crypsinus engleri 87 0.86 0.73 471 554 ‐54 ‐44 0.9496 Fern 39 Ctenopteris curtisii 95 0.98 0.71 625 556 ‐88 ‐38 0.9502 Fern 40 Ctenopteris merrittii 5 0.98 0.94 1072 926 ‐88 ‐69 0.9788 Fern 41 Ctenopteris obliquata 80 0.89 0.91 554 385 ‐52 ‐86 0.9399 Fern Ctenopteris 42 13 0.89 0.71 436 531 ‐46 ‐54 0.9442 Fern subfalcata Ctenopteris 43 10 0.87 0.91 ‐37 ‐751 34 ‐50 0.9949 Fern tenuisecta -CONTINUED-

150

APPENDIX 2

44 Cymbidium dayanum 52 0.86 0.68 376 417 ‐4 ‐19 0.8845 Orchid Cymbidium 45 8 0.98 0.88 658 603 ‐93 ‐63 0.9690 Orchid floribundum 46 Davallia formosana 117 0.99 0.76 496 387 ‐86 ‐51 0.9336 Fern 47 Davallia mariesii 410 0.85 0.71 622 550 ‐26 ‐13 0.8465 Fern 48 Davallia solida 28 0.68 0.78 ‐53 ‐128 89 314 0.9572 Fern Dendrobium 49 21 0.92 0.85 866 617 ‐78 ‐71 0.9458 Orchid chameleon Dendrobium 50 44 0.93 0.70 432 309 ‐80 ‐59 0.9182 Orchid chryseum 51 Dendrobium falconeri 17 1.00 0.82 ‐36 196 ‐93 ‐75 0.9921 Orchid Dendrobium 52 6 0.89 0.90 ‐518 ‐492 ‐57 ‐79 0.9730 Orchid linawianum Dendrobium 53 119 0.88 0.81 ‐11 ‐242 17 15 0.9105 Orchid moniliforme 54 Dendrobium somae* 17 0.85 0.60 285 88 145 24 0.9648 Orchid Diploprora 55 50 0.79 0.73 ‐246 ‐300 136 86 0.9365 Orchid championii 56 Dischidia formosana* 132 0.89 0.80 631 551 ‐56 ‐48 0.9028 Dico Drymotaenium 57 20 0.91 0.51 256 158 ‐55 ‐6 0.9485 Fern miyoshianum 58 Drynaria fortunei 85 0.98 0.77 1137 545 ‐62 ‐36 0.9517 Fern Elaphoglossum 59 12 0.86 0.72 492 461 ‐71 ‐45 0.9650 Fern callifolium Elaphoglossum 60 9 1.00 0.97 ‐654 ‐160 ‐96 ‐95 0.9752 Fern luzonicum Elaphoglossum 61 33 0.87 0.69 347 523 ‐42 ‐37 0.9571 Fern marginatum* Elaphoglossum 62 59 0.95 0.91 964 951 ‐90 ‐86 0.9429 Fern yoshinagae 63 Epigeneium fargesii 8 0.99 0.85 ‐1497 232 ‐87 ‐54 0.9432 Orchid Epigeneium 64 29 0.88 0.60 583 344 ‐67 ‐4 0.9171 Orchid nakaharae* 65 Eria corneri 90 0.90 0.80 746 521 ‐23 ‐10 0.9105 Orchid 66 Eria japonica 29 0.99 0.83 603 579 ‐93 ‐69 0.9162 Orchid 67 Eria ovata 75 0.75 0.69 764 508 ‐23 ‐43 0.9249 Orchid 68 Eria tomentosiflora 53 0.77 0.52 258 235 1 ‐22 0.9339 Orchid Flickingeria 69 6 0.99 1.00 793 715 ‐49 ‐71 0.9966 Orchid tairukounia* 70 Gastrochilus ciliaris 7 0.98 0.87 283 440 ‐86 ‐66 0.9817 Orchid -CONTINUED-

151

APPENDIX 2

Gastrochilus 71 62 0.99 0.65 360 362 ‐95 ‐37 0.8746 Orchid formosanus Gastrochilus 72 46 0.88 0.57 497 308 ‐64 ‐5 0.9207 Orchid fuscopunctatus* 73 Gastrochilus hoii* 7 0.93 0.86 ‐255 17 65 ‐73 0.9899 Orchid Gastrochilus 74 37 0.83 0.74 836 781 ‐17 13 0.9184 Orchid japonicus Gastrochilus 75 21 0.98 0.75 434 233 ‐96 ‐41 0.9891 Orchid matsudai* Gastrochilus 76 12 0.96 0.78 856 589 ‐90 ‐77 0.9352 Orchid rantabunensis Gastrochilus 77 14 0.97 0.96 660 738 ‐92 ‐94 0.9503 Orchid raraensis* 78 Gonocormus minutus 44 0.97 0.89 1197 776 ‐74 ‐75 0.8816 Fern Goodyera 79 16 0.97 1.00 845 530 ‐93 ‐99 0.9651 Orchid bilamellata* 80 Grammitis congener 22 0.96 0.94 902 476 ‐89 ‐93 0.9549 Fern 81 Grammitis fenicis 13 0.88 0.79 908 692 ‐68 ‐59 0.9610 Fern 82 Grammitis jagoriana 5 0.84 0.80 ‐385 ‐388 ‐9 ‐66 0.9887 Fern 83 Grammitis nuda* 5 1.00 1.00 944 885 ‐83 ‐90 0.9982 Fern Grammitis 84 13 0.97 0.95 1090 1000 ‐89 ‐87 0.9850 Fern reinwardtia Holcoglossum 85 23 0.96 0.70 611 478 ‐85 ‐45 0.9461 Orchid quasipinifolium 86 Hoya carnosa 376 0.75 0.46 269 217 ‐8 7 0.8848 Dico Humata 87 15 1.00 0.86 549 304 ‐85 ‐33 0.9641 Fern chrysanthemifolia 88 Humata griffithiana 37 0.81 0.56 0 325 ‐46 ‐15 0.9108 Fern 89 Humata repens 20 0.86 0.81 342 346 ‐69 ‐67 0.9290 Fern 90 Humata trifoliata 52 0.90 0.79 956 481 ‐66 ‐61 0.9060 Fern 91 Humata vestita 8 0.76 0.51 ‐65 19 109 2 0.9504 Fern Hydrangea 92 354 0.90 0.67 671 552 ‐63 ‐39 0.8978 Dico integrifolia Hymenophyllum 93 73 0.88 0.78 507 280 ‐64 ‐70 0.9249 Fern barbatum Hymenophyllum 94 10 0.78 0.61 855 600 ‐4 ‐18 0.9354 Fern fimbriatum Hymenophyllum 95 10 0.92 0.68 522 489 ‐57 ‐20 0.9258 Fern simonsianum Lemmaphyllum 96 125 0.98 0.80 ‐1080 531 ‐89 ‐65 0.9555 Fern diversum -CONTINUED-

152

APPENDIX 2

Lemmaphyllum 97 922 0.85 0.78 1045 871 ‐26 ‐22 0.8504 Fern microphyllum 98 Lepisorus clathratus 15 0.95 0.83 ‐582 22 ‐80 ‐52 0.9841 Fern 99 Lepisorus kawakamii* 67 0.82 0.53 240 239 ‐58 ‐20 0.9130 Fern 100 Lepisorus megasorus* 87 0.91 0.71 468 439 ‐42 ‐36 0.9210 Fern Lepisorus 101 170 0.80 0.63 637 629 ‐33 ‐13 0.8911 Fern monilisorus* Lepisorus 102 60 0.89 0.63 75 290 ‐48 ‐39 0.9464 Fern morrisonensis Lepisorus 103 41 0.94 0.58 598 286 ‐76 9 0.9273 Fern obscurevenulosus Lepisorus 104 87 0.89 0.57 140 102 ‐28 8 0.9491 Fern pseudoussuriensis* Lepisorus 105 21 0.93 0.55 132 55 ‐30 ‐5 0.9850 Fern suboligolepidus Lepisorus 106 362 0.95 0.80 923 879 ‐68 ‐56 0.8690 Fern thunbergianus 107 Lepisorus tosaensis 30 0.90 0.58 336 146 ‐61 ‐3 0.9449 Fern 108 Leucostegia immersa 26 0.94 0.70 468 379 ‐67 ‐39 0.9582 Fern 109 Liparis bootanensis 181 0.82 0.74 ‐418 ‐299 47 1 0.9208 Orchid 110 Liparis caespitosa 42 0.79 0.73 ‐359 ‐404 11 ‐9 0.9186 Orchid 111 Liparis condylobulbon 30 0.81 0.68 217 231 11 9 0.9170 Orchid 112 Liparis elliptica 62 0.88 0.85 709 544 31 ‐40 0.9028 Orchid 113 Liparis grossa 10 0.94 0.79 204 147 882 275 0.9711 Orchid 114 Liparis nakaharai* 85 0.89 0.85 970 1037 ‐3 ‐15 0.8945 Orchid 115 Liparis somai* 5 0.81 0.72 227 452 232 54 0.9678 Orchid 116 Liparis viridiflora 9 0.95 0.65 694 343 ‐60 ‐1 0.9427 Orchid Lomariopsis 117 26 0.78 0.66 42 49 126 90 0.9428 Fern spectabilis Loxogramme 118 51 0.96 0.63 525 384 ‐89 ‐50 0.9308 Fern formosana Loxogramme 119 14 0.85 0.54 ‐71 86 ‐78 ‐46 0.9038 Fern grammitoides Loxogramme 120 49 0.77 0.58 121 322 ‐22 ‐37 0.9120 Fern remotefrondigera* Loxogramme 121 166 0.87 0.74 926 679 ‐33 9 0.8925 Fern salicifolia 122 Luisia cordata* 7 0.61 0.31 12 23 ‐18 ‐4 0.9763 Orchid 123 Luisia megasepala* 11 0.85 0.62 164 333 30 48 0.9584 Orchid -CONTINUED-

153

APPENDIX 2

124 Luisia teres 25 0.75 0.66 300 418 92 55 0.9027 Orchid Lycopodium 125 14 0.77 0.61 456 385 85 59 0.9005 Fern carinatum Lycopodium 126 8 0.80 0.60 486 410 46 13 0.9378 Fern cunninghamioides 127 Lycopodium fargesii 61 0.83 0.68 556 556 ‐42 ‐32 0.8585 Fern 128 Lycopodium fordii 191 0.81 0.68 703 576 ‐25 ‐3 0.9024 Fern Lycopodium 129 31 0.82 0.62 14 58 ‐5 ‐25 0.9232 Fern phlegmaria Lycopodium 130 29 0.85 0.73 ‐15 188 ‐72 ‐40 0.9294 Fern salvinioides 131 Lycopodium sieboldii 27 0.91 0.89 158 533 98 ‐74 0.9195 Fern Lycopodium 132 19 0.96 0.96 1143 1086 ‐58 ‐88 0.9479 Fern squarrosum Lycopodium 133 21 0.86 0.80 ‐575 323 ‐52 ‐68 0.9391 Fern taiwanense 134 Lysionotus pauciflorus 323 0.84 0.70 652 565 ‐38 ‐32 0.8982 Dico 135 Mecodium badium 111 0.96 0.96 1151 742 ‐81 ‐84 0.9496 Fern 136 Mecodium javanicum 16 0.92 0.86 891 766 ‐78 ‐67 0.9566 Fern Mecodium 137 23 1.00 0.99 585 ‐162 ‐98 ‐97 0.9514 Fern oligosorum Mecodium 138 283 0.86 0.75 915 780 ‐41 ‐38 0.8960 Fern polyanthos 139 Medinilla formosana* 39 0.55 0.59 ‐99 227 ‐32 ‐2 0.9865 Dico Microsorium 140 649 0.90 0.79 923 768 ‐66 ‐46 0.8478 Fern buergerianum Microsorium 141 42 0.95 0.87 866 701 ‐90 ‐77 0.9011 Fern dilatatum Microsorium 142 145 0.85 0.68 87 1 47 68 0.9151 Fern punctatum Microtatorchis 143 5 1.00 0.89 830 471 ‐84 ‐15 0.9836 Orchid compacta Microtrichomanes 144 11 0.95 0.80 738 603 ‐80 ‐53 0.9324 Fern nitidulum 145 Oberonia arisanensis 51 0.90 0.79 599 592 ‐56 ‐55 0.8553 Orchid 146 Oberonia caulescens 71 0.83 0.61 660 470 ‐48 ‐17 0.8805 Orchid 147 Oberonia gigantea* 10 0.79 0.51 535 431 ‐23 ‐12 0.9191 Orchid 148 Oberonia japonica 17 0.83 0.71 780 655 ‐15 ‐27 0.9420 Orchid 149 Oberonia pumila* 7 0.81 0.56 291 394 41 9 0.9399 Orchid 150 Oberonia rosea 5 0.61 0.41 24 11 17 ‐14 0.9888 Orchid -CONTINUED-

154

APPENDIX 2

Oberonia 151 5 0.93 0.82 257 257 169 35 0.9939 Orchid seidenfadenii* 152 Oleandra wallichii 17 0.88 0.73 ‐147 ‐10 45 45 0.9567 Fern 153 Ophioderma pendula 81 0.89 0.80 621 505 ‐23 ‐38 0.9300 Fern Pachycentria 154 104 0.94 0.82 ‐104 213 ‐73 ‐26 0.9430 Dico formosana* Pentapanax 155 9 0.84 0.51 158 243 ‐65 ‐45 0.9073 Dico castanopsisicola* 156 Peperomia japonica 276 0.81 0.57 540 444 ‐17 ‐10 0.8403 Dico Peperomia 157 28 0.76 0.56 ‐117 ‐143 44 53 0.9411 Dico nakaharai* 158 Peperomia reflexa 209 0.83 0.58 100 282 ‐46 ‐27 0.8976 Dico 159 Peperomia sui* 28 0.99 0.76 ‐168 151 ‐97 ‐64 0.9281 Dico Phalaenopsis 160 6 0.85 0.77 158 70 471 317 0.9829 Orchid aphrodite 161 Pholidota cantonensis 45 0.95 0.92 957 701 ‐82 ‐86 0.9275 Orchid 162 Phreatia formosana 13 0.81 0.60 158 167 50 ‐29 0.8922 Orchid 163 Phreatia morii* 15 0.94 0.71 813 538 ‐71 ‐17 0.9592 Orchid 164 Phreatia taiwaniana* 7 0.97 0.91 1020 822 ‐83 ‐64 0.9514 Orchid Pileostegia 165 390 0.82 0.71 747 695 ‐44 ‐42 0.8901 Dico viburnoides Pleuromanes 166 10 0.76 0.69 578 628 ‐58 ‐53 0.9488 Fern pallidum Polypodium 167 139 0.95 0.81 361 492 ‐56 ‐51 0.9346 Fern amoenum 168 Polypodium argutum 100 0.96 0.86 605 447 ‐65 ‐36 0.9670 Fern Polypodium 169 71 0.88 0.86 985 813 ‐35 ‐41 0.8687 Fern formosanum Polypodium 170 8 0.95 0.68 253 233 ‐25 36 0.9805 Fern microrhizoma Polypodium 171 50 0.75 0.64 463 554 9 ‐31 0.9210 Fern raishanense* Polypodium 172 35 0.89 0.76 288 495 ‐54 ‐40 0.9480 Fern transpianense* Pomatocalpa 173 12 0.84 0.48 203 135 ‐31 8 0.9084 Orchid acuminata* 174 Procris laevigata 175 0.96 0.80 830 594 ‐75 ‐52 0.9109 Dico 175 Prosaptia contigua 101 0.92 0.82 912 796 ‐51 ‐41 0.9463 Fern Pseudodrynaria 176 418 0.92 0.77 780 583 ‐52 ‐38 0.8644 Fern coronans 177 Psilotum nudum 137 0.73 0.61 385 197 ‐8 ‐7 0.9230 Fern -CONTINUED- 155

APPENDIX 2

178 Pyrrosia adnascens 136 0.82 0.66 193 233 ‐16 87 0.9079 Fern 179 Pyrrosia gralla 50 0.99 0.67 106 358 ‐97 ‐59 0.9564 Fern 180 Pyrrosia linearifolia 117 0.94 0.77 140 324 ‐60 ‐47 0.9373 Fern 181 Pyrrosia lingua 591 0.91 0.73 819 718 ‐66 ‐37 0.8259 Fern 182 Pyrrosia matsudae* 30 1.00 0.77 383 270 ‐99 ‐65 0.9643 Fern 183 Pyrrosia polydactylis* 233 0.86 0.67 416 524 ‐3 6 0.9074 Fern 184 Pyrrosia sheareri 194 0.84 0.61 641 397 ‐59 ‐35 0.9356 Fern Pyrrosia 185 21 0.87 0.68 ‐188 91 ‐37 ‐3 0.9732 Fern transmorrisonensis* Rhododendron 186 64 0.88 0.66 549 459 ‐45 ‐28 0.9062 Dico kawakamii* Saxiglossum 187 14 1.00 0.93 661 ‐127 ‐89 ‐89 0.9907 Fern angustissimum Schoenorchis 188 9 0.31 0.32 ‐3 ‐17 20 4 0.9574 Orchid vanoverberghii Scleroglossum 189 9 0.95 0.96 ‐742 ‐775 ‐15 ‐81 0.9820 Fern pusillum 190 Selaginella delicatula 1083 0.86 0.65 724 440 ‐25 ‐17 0.8002 Fern 191 Selaginella involvens 413 0.87 0.70 929 749 ‐58 ‐35 0.8660 Fern Staurochilus 192 22 0.90 0.76 ‐36 ‐75 524 312 0.9638 Orchid luchuensis 193 Sunipia andersonii 41 0.90 0.66 297 215 ‐62 ‐41 0.9498 Orchid Thrixspermum 194 5 0.94 0.81 123 494 193 15 0.9750 Orchid eximium Thrixspermum 195 12 0.66 0.47 9 56 64 ‐14 0.9236 Orchid fantasticum Thrixspermum 196 27 0.80 0.48 203 182 15 38 0.9344 Orchid formosanum Thrixspermum 197 8 0.87 0.74 264 153 ‐38 ‐7 0.9839 Orchid laurisilvaticum 198 Thrixspermum pensile 11 0.87 0.62 238 237 20 61 0.9699 Orchid Thrixspermum 199 16 0.97 0.86 14 60 ‐84 ‐69 0.9467 Orchid saruwatarii* Thrixspermum 200 8 0.78 0.68 304 248 ‐7 152 0.9578 Orchid subulatum 201 Trichoglottis rosea 10 0.79 0.76 554 369 7 7 0.9816 Orchid Vaccinium 202 dunalianum var. 126 0.96 0.74 856 596 ‐70 ‐29 0.9323 Dico caudatifolium* Vaccinium 203 210 0.95 0.78 651 473 ‐86 ‐65 0.9257 Dico emarginatum* -CONTINUED-

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APPENDIX 2

204 Vaginularia paradoxa 7 0.71 0.71 ‐54 ‐18 65 88 0.9884 Fern Vandenboschia 205 360 0.88 0.69 617 566 ‐55 ‐37 0.8819 Fern auriculata Vandenboschia 206 33 0.78 0.69 982 725 ‐27 ‐23 0.9012 Fern radicans Vittaria anguste‐ 207 205 0.85 0.70 320 322 ‐45 ‐35 0.8983 Fern elongata 208 Vittaria flexuosa 421 0.81 0.65 418 522 ‐22 ‐30 0.8615 Fern 209 Vittaria taeniophylla 58 0.64 0.42 ‐22 22 ‐33 ‐17 0.9221 Fern 210 Vittaria zosterifolia 158 0.84 0.73 631 379 ‐25 ‐22 0.9070 Fern 211 Xiphopteris okuboi 88 0.88 0.84 945 880 ‐42 ‐58 0.9617 Fern

157

158

SUMMARY

From 1997 to 1998, a strong El Niño event caused a dramatic decline of epiphytic populations in NE Taiwan (pers. observ.). Looking back, this incident has triggered my interest in the response of epiphytes to climate change, which is the main topic of this dissertation. At the time of the El Niño event, for Taiwan virtually no information was available yet on the floristic composition of the epiphyte flora, the biogeography of epiphytes, and the regional epiphyte distribution patterns. Moreover, the ecophysiology of Taiwanese epiphytes had been little studied, in particular in relation to global warming with presumed accompanying changes in

CO2 availability and solar insulation. Hence, conservationists were far removed from making a dependable assessment of the impact of climatic change on epiphyte communities in Taiwan.

Taiwan is a 36,000 km2 island in East Asia (21°45'–25°56'N and 119°18'E–124°34'E). About 70% of the island is covered by mountains of 1000 up to 3952 m asl in height, with a dominant central range along the island’s long axis. Annual rainfall ranges from 1,000 to over 6,000 mm depending on the prevailing wind directions.

The general aim of this study is to get insight in the response of Taiwanese epiphytes to climate change. More in detail, the following hypotheses were tested: 1) the composition of epiphyte flora is similar to other tropical areas; 2) the epiphyte flora is a mixture of that of adjacent floristic regions, influenced by prevailing winds; 3) epiphytes show a mid-elevation peak in richness that is better explained by environmental factors than by the mid-domain effect; 4) The evolution of Crassulacean Acid Metabolism (CAM) in humid forest epiphytes occurred in response to CO2 availability; 5) in Asplenium nidus, the photosynthetic capacity is greater for the leaf surface that receives more insolation during a day; 6) there exists intraspecific variation of a widespread epiphytic fern Asplenium antiquum which determines its responses to changing climate; 7) epiphyte distribution are correlated with forest types; 8) certain epiphytic species and forest types are relatively susceptible to climate change.

To test the various hypotheses, descriptive, experimental (laboratory and field), and modelling studies were performed. A descriptive study, based on botanical collections in herbaria, helped to obtain insight in the current floristic composition, distribution and richness patterns of vascular epiphytes (hypothesis 1-3, chapters 2,3). Laboratory experiments and in situ measurements gained insight in the hypothesized evolution of CAM in response to diurnal changes in air CO2 concentration (Hoya carnosa) and in the photosynthetic capacity of fern leaves (Asplenium nidus) under different conditions (hypothesis 4,5, chapters 4,5). A field experiment assessed the occurrence of adaptation of populations of a widespread epiphytic fern (Asplenium antiquum) to simulated climate-change conditions (hypothesis 6, chapter 6). Finally, a modelling approach was performed to assess epiphyte distribution patterns

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SUMMARY

(hypothesis 3, chapter 3) and climate change impacts on forests and associated vascular epiphytes (hypothesis 7,8, chapter 7).

Chapter 2. Composition and phytogeography of the epiphyte flora

By consulting herbarium specimens, literature records, and field observations, an epiphyte checklist was compiled comprising 336 vascular species (105 genera of 24 families). The Epiphyte-Quotient (i.e. the proportion of epiphytic species) was only 8%. Presumably, frequent tropical storms (typhoons) have contributed to the reduced epiphyte diversity in Taiwan. Similar to epiphytic flora’s in other tropical regions, our checklist is dominated by few families, especially ferns (171 spp) and orchids (120 spp). Epiphyte endemism was high (21.3%), with half of the endemic species being orchids. Regarding epiphyte phytogeography, the total epiphyte flora exhibited a similar affinity to Malesian, Eastern Asiatic and Indochinese regions, yet epiphytic orchids shared most species with Indo-China, which likely may be attributed to prevailing winds.

Chapter 3. Epiphyte distribution pattern and explanatory factors

Using 39,084 unique botanical records, the elevational distribution pattern of over 300 epiphytic species was explored. The result showed a richness peak between 500 and 1500m asl that could not be explained by the mid-domain effect, suggesting environmental factors mostly accounting for epiphyte distribution. The overall epiphyte richness patterns were modelled using species distribution models, software MaxEnt. The modelled result not only corroborated the position of the mid-elevation peak in epiphyte richness, it also identified two regions with exceptionally high species richness in mid-elevations. The epiphyte hotspots are probably related to the direction of prevailing winds. Exploratory ordination analyses indicated two factors, elevation-related temperature and precipitation, which were most influential for epiphyte distribution. However, subcategories demonstrated different thermal preferences; for instance, hemi-epiphytes were most abundant in the lowland tropical forest whilst epiphytic ferns showed a preference for increasing elevations. In contrast to predictions by the Rapoport Effect hypothesis, the ordination analysis also showed that the degree of thermal specialisation increased with elevation, suggesting that highland species are especially vulnerable to global warming. Finally, in a partial ordination analysis controlling for all other variables, typhoons were shown to exert a significant influence on the distribution of epiphytes.

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SUMMARY

Chapter 4. CO2 availability and the evolution of CAM in the epiphyte Hoya carnosa

Twenty CAM plants of Hoya carnosa were selected to compare the acid accumulations and stable carbon isotope ratios of their leaves under two habitat conditions. Ten in host trees that grow in intact, dense stands of forest (closed canopies), and ten in hosts with few neighbour trees (open canopies). We found that the air CO2 concentration was significantly higher (40-60 µmol mol-1) at night than during the day, and was higher in closed canopies than in open canopies at night, presumably the result of host-respired CO2 added to the canopy air. However, the carbon isotope ratio of H. carnosa was not substantially lower than those of many other CAM plants, suggesting that the surplus CO2 released by host trees to the atmosphere at night was not an importance CO2 source for these CAM plants. In addition, in vitro experiment showed an appreciable daytime CO2 uptake in H. carnosa, which should even lower the carbon isotope values of the species. Overall, the results indicated that host-respired CO2 does not contribute CO2 budget of canopy epiphytes, hence does not support the hypothesis that CAM has evolved in epiphytes in response to diurnal changes in air CO2 concentration rather than water conservation.

Chapter 5. Plasticity of photosynthetic capacity in the epiphytic fern Asplenium nidus

CO2 exchange rates of leaves in an epiphytic ferns were measured in situ to compare the difference of photosynthetic capacity between two leaf sides in relation to sunlight exposure. Three orientations of leaves with different patterns in sunlight exposure were selected, namely, vertical, angled and horizontal leaves spacing from inner to outer rings in Asplenium nidus, a fern of a rosette growth form. Except the vertically oriented leaves, the results indicated that photosynthetic rates were higher when the side of the leaf that typically received more direct isolation was illuminated during the measurement. Judging from equal stomatal conductances and accompanying transpiration rates, the higher CO2 uptake rates were attributed to a greater biochemical capacity for photosynthesis. The study revealed the physiological plasticity within epiphytes in relation to their diverse microclimate conditions.

Chapter 6. Adaptation of a widespread epiphytic fern, Asplenium antiquum, to simulated climate change

A two-year reciprocal transplant field experiment along an altitudinal gradient was conducted to investigate the adaptive response of juvenile plants of the widespread epiphytic fern Asplenium antiquum to simulated climate change conditions. The experiment results showed a

161

SUMMARY strong site effect between the three altitudinal sites at 600, 1100 and 1950 m asl on both the growth and survivorship of juvenile A. antiquum. Under the more extreme climate conditions at the highland site, the local population was clearly better adapted, evidenced by their significantly higher survival than the other two populations. The results suggested that intraspecific genetic diversity should be considered when assessing the potential impact of climate change on species.

Chapter 7. Modelling climate change impacts on forests and associated epiphytes

Hierarchical species distribution models (SDMs) were used to assess climate change impacts on forests and 237 vascular epiphyte species in Taiwan. By (1) incorporating dispersal limitation, tree persistence, and non-climatic factors into models, and (2) considering biotic interactions between epiphytes and host trees, a novel approach was developed to improve SDMs' accuracy and realism. The modelled results suggested that epiphyte distributions highly depended on forest compositions. In the model results, the annual means and the variances of the climate variables exerted an equal influence on species distributions, and non-climatic factors tended to retain their influence under climate change conditions. Our model also indicated certain forest types (e.g. Cypress and Picea forests) and certain thermal- or hydro- sensitive species are relatively more vulnerable to projected scenarios of climate change on the island.

In conclusion, the descriptive study of epiphytes on Taiwan has shown that its epiphyte flora is typical for tropical island biota, having relatively low diversity compared to mainland areas, yet showing high endemism, and sharing a low number of dominating groups, especially ferns and orchids. The relatively low diversity and the low contribution of epiphytes to the total vascular flora is, presumably, at least partly, explained by frequent large scale typhoon disturbances. Modelling showed that the altitudinal epiphyte distribution pattern was mostly accounted for by environmental factors rather than a null model of geometric constraints. However, laboratory experiments also showed that epiphytes may have a substantial degree of physiological plasticity in response to the diverse habitat of forest canopies. In addition, a field experiment indicated an intraspecific genetic adaptation to elevation for a widespread species. Information on physiological plasticity along with genetic adaptation is essential for assessing the climate change impacts on epiphyte biodiversity. Lastly, it is concluded that the mid- elevation Cypress and Picea forests that have a large number of niche-specialized epiphytic species deserve special attention for conservation purposes.

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總結

台灣位於東亞(北緯 21°45'–25°56'N，東經 119°18'E–124°34'E)，是一個面積約

3 萬 6 千平方公尺的島嶼，中央山脈由北至南縱貫全島，約有 70%的陸地皆由海拔

1000 公尺以上的山地所覆蓋(最高峰玉山 3952 公尺)，年雨量則由 1000 至 6000 公厘不

等。筆者自 1996 年便在台灣東北部的福山保護區進行附生植物的調查，於碩士論文

研究期間適逢 1997 至 1998 的強烈聖嬰現象，觀察到樣區中附生植物族群有大規模的

乾枯死亡，也因此激發筆者想要了解未來氣候變遷將會對附生植物族群造成的影響，

然而，當時台灣對於附生植物的研究尚少，尤其是本地附生植物的組成、分布以及

生理生態方面的研究報告皆付之闕如，更無從推論附生植物在氣候變遷下，面臨溫

度、雨量甚或二氧化碳濃度變化的反應，遑論相關保育政策的制定了，因此本研究

的目標便是針對台灣附生植物進行如前所述的基礎研究，並進一步了解氣候變遷可

能對附生植物造成的影響。

本論文針對以下幾個假設加以檢視驗證: 1. 台灣的附生植物組成與其他熱帶

地區類似；2. 台灣的附生植物組成受季節風向的影響，並具有鄰近植物區系的複合

特徵；3. 台灣附生植物的多樣性在中海拔呈現高峰，此現象與環境因子的相關性勝

過地形上的中域效應(Mid-domain effect)；4. 潮濕森林中景天代謝(Crassulacean acid metabolism)的演化起源與二氧化碳的可得性有關；5. 台灣山蘇(Asplenium nidus)吸收較

多日照的葉片，其光合作用潛力也較大；6. 海拔分布廣泛的山蘇(Asplenium antiquum)，

不同族群存在著種內變異，也對氣候變遷產生不同的反應；7. 附生植物的分布與植

被類型相關；8. 某些附生植物及植被類型對氣候變遷較為敏感。

為了測試上述的假設，本論文的研究方法包括敘述統計、野外實驗、實驗室

試驗及電腦模式預測。首先筆者根據田野觀察，編製台灣的附生植物名錄，並整理

全台灣各大標本館採集紀錄，以分析附生植物的組成、多樣性及分布型式(假設 1-3，

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總結

章節 2 與 3)。田野及試驗室的試驗則包含：量測毬蘭(Hoya carnosa)於森林中時空間變

化下、不同二氧化碳濃度的光合代謝產物，以證實景天代謝的演化動力(假設 4，章

節 4)；量測台灣山蘇(Asplenium nidus)葉片於不同日照環境下的光合作用潛力(假設 5，

章節 5)。針對山蘇(Asplenium antiquum)的小苗進行田野試驗，以模擬氣候變遷對本物種

可能造成的影響(章節 6，假設 6)。最後以電腦模式建立台灣的附生植物分布型式(假

設 3，章節 3)以及模擬附生植物在氣候變遷下的反應(假設 7 與 8，章節 8)。

第 2 章：台灣維管束附生植物的組成及親緣地理

經檢視標本館的標本、文獻紀錄以及野外觀察，筆者編製了台灣的維管束附

生植物名錄，此名錄共包含 336 個物種，分屬於 105 個屬及 24 個科，並得出台灣的

附生植物商數(Epiphyte-Quotient，附生植物占全部植物種數的比例)為 8%，此比例明

顯低於世界平均水準的 10%，推測夏秋兩季頻繁侵襲的颱風是減低附生植物多樣性

的原因之一。與其他熱帶區域的組成類似，台灣的附生植物的組成偏重在少數分類

群，其中蕨類植物占了 171 種，而蘭科植物佔了 120 種，特有種比例偏高(21.3%)，其

中有一半都是蘭科植物。台灣附生植物的親緣地理關係與馬來西亞、東亞及中南半

島等植物區系皆有密切關係，其中蘭科植物與中南半島植物的親緣最為相近，推測

可能與夏季旺盛的西南氣流有關。

第 3 章：台灣附生植物的分布及可能的影響因子

藉由收集標本館藏及訪談植物學家，筆者編製了附生植物資料庫共包含

39084 筆採集紀錄。分析將近 300 個物種的採集紀錄，顯示物種最豐富的區間位於

500-1500 公尺的中海拔，然而此中海拔物種特別豐富的現象，經統計檢測後無法以中

域效應解釋，顯示附生植物的豐富度與環境因子較為相關。此外，筆者使用物種分

布模式工具 MaxEnt 及相關的環境因子來模擬台灣附生植物的分布，模式結果與前述

利用採集紀錄分析的結果相同，也顯示附生植物的多樣性在中海拔到達峰值，且模

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總結

式結果同時也指出，有 2 個位於台灣北部及中部的中海拔地理區，擁有較高的附生

植物多樣性，推測這 2 個附生植物熱點的形成原因，可能與盛行風向相關。序列分

析(Ordination analysis)結果顯示，年雨量以及與海拔相關的年均溫是影響附生植物分

布最主要的因子，不過不同的分類群對溫度的偏好也有差異，例如半附生植物多生

長在低海拔的溪谷，而附生蕨類則喜愛涼爽的山地氣候。序列分析結果也指出，台

灣的附生植物對溫度敏感(Thermal specialisation)的程度，隨海拔上升而增加，此趨勢

顯然與 Rapoport 法則的假設相反，而在全球暖化的趨勢下，台灣高海拔物種可能將

遭受比較大的威脅。最後，局部序列分析(Partial ordination)顯示颱風對附生植物的分

布造成顯著的影響。

第 4 章：潮濕森林中景天代謝的演化起源與二氧化碳的可得性

本研究選取了位於 2 種不同棲地環境的毬蘭樣本共 20 株，其中 10 株附著在

茂密的森林中，另外 10 株則生長在零星分布於空曠區域的大樹上。量測顯示夜間大

氣中的二氧化碳濃度顯著高於白晝(差距約在 40-60 µmol mol-1)，且茂密森林裡的二氧

化碳濃度也高於空曠區域，推測為周遭樹木夜間的呼吸作用釋放出二氧化碳所致。

然而針對毬蘭葉片檢測碳-13，卻發現樣本內的穩定性同位素濃度並未顯著低於其它

景天代謝植物，顯示毬蘭並未充分利用宿主在夜間所釋出的二葉化碳作為碳源，此

外，控制實驗顯示，毬蘭並非嚴格的景天代謝植物，在白晝期間也會進行 C3 的光合

作用，而因此更進一步降低細胞內的碳-13 濃度。以上種種結果顯示，毬蘭雖然是分

布在潮濕森林裡的附生植物，其景天代謝的演化動力，可能還是為了降低水分散失，

而不是為了利用宿主在夜間所釋放出來多餘的二氧化碳。

第 5 章：台灣山蘇葉片光合作用潛能的可塑性(plasticity)

台灣山蘇是一種葉片呈蓮座狀排列的大型附生蕨類，本研究選取從內圈至外

圈 3 種不同傾斜角度的葉片(垂直、45 度角、水平)，野地量測不同天然光照條件下，

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總結

葉片兩面的二氧化碳交換率。結果顯示，除了最內圈的垂直葉片以外，接收較多光

照時數的山蘇葉面基本上擁有較高的光合作用速率，由於所有量測樣本皆呈現相似

的氣孔導度(Stomatal conductances)及蒸散率(Transpiration rates)，推測差異歸因於受較

長日照葉面具有較高的生化承載力(Biochemical capacity)，本試驗結果顯示附生植物的

生理可塑性與其微環境的高度變異有極大相關性。

第 6 章：移栽(Reciprocal transplantation)試驗模擬山蘇對氣候變

遷的適應性

山蘇在台灣是一種廣布種植物，本研究以為期兩年的移栽試驗，模擬山蘇的

小苗對氣候變遷的適應性。研究結果顯示，不同海拔種源的山蘇小苗，在低、中、

高海拔(600、1100 與 1950 公尺)樣區呈現顯著不同的生長與存活率，在生長環境最為

極端的高海拔樣區，種源來自於當地的山蘇小苗具有較佳的適應力，顯然比中、低

海拔種源小苗擁有更高的存活率。本研究顯示在評估氣候變遷對物種的潛在衝擊時，

必須一併考慮種內遺傳多樣性對物種的環境適應所造成的影響。

第 7 章：利用物種分布模式(Species distribution model)模擬氣候

變遷對附生植物以及森林植群的影響

本研究改良傳統物種分布模式，採用階層式(hierarchical)的模式建立流程，來

評估在未來氣候變遷條件下，現有的森林植群以及 237 種真附生植物，將在分布上產

生何種變化? 為了增進物種分布模式於氣候變遷預測的準確性及真實性，本研究考量

樹木的傳播距離以及樹木在不適宜環境下的耐受性，此外還將地形、坡向等非氣候

性的環境因子一併納入模式建立。由於附生植物的分布受植被類型影響甚鉅，在模

擬氣候變遷下附生植物的分布時，亦將未來的森林分布作為環境因子納入模式。結

果顯示，氣候條件的平均值與季節性變異對物種分布有同樣重要的影響，而地形等

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總結

非氣候性因子，則在氣候變遷的條件下，對物種未來的分布維持同樣的影響力。本

研究指出若干植被類型(例如：雲杉、檜木)以及某些對環境溫度及水分變化敏感的附

生植物，在未來氣候變遷的條件下將會受到較大的衝擊。

結論

歸納本研究的發現如下，台灣附生植物的組成具典型熱帶島嶼特徵，相對於大陸塊，

擁有較高的特有種比率及較低的物種數，且為少數分類群(蕨類及蘭科植物)所支配。

序列分析結果顯示，頻繁侵襲的颱風對台灣附生植物的分布有顯著的影響，影響程

度雖然還不明朗，但台灣附生植物佔整體植物誌偏低的現象可能與颱風的干擾有關。

物種分布模式結果顯示，台灣附生植物的海拔分布，主要受環境因子(溫度及雨量)的

影響，而非單純幾何限制所造成空間分布上的中域效應。然而本研究也以實驗結果

證實，附生植物具有卓越的生理可塑性以適應樹冠層多變的棲地環境。此外，移栽

試驗顯示附生植物的廣布種，其種內的基因變異可能會影響物種對氣候變遷的適應

性，應在保育評估中納入考量。最後，本研究指出中海拔的檜木林及雲杉等霧林帶，

擁有許多分布狹隘的特有種附生植物，未來應特別關注氣候變遷對其造成的衝擊。

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168

SAMENVATTING

Een sterk El Niño effect in de winter van 1997 had een dramatische achteruitgang van epifyten op Taiwan tot gevolg (pers. observatie). Dit voorval heeft achteraf gezien mijn belangstelling voor de studie van de invloed van klimaatverandering op epifytische populaties gewekt en de resultaten van die studie vormen een belangrijk onderdeel van deze dissertatie. Ten tijde van de El Niño gebeurtenis was er vrijwel nog geen informatie beschikbaar over de floristische samenstellingen en verbreiding van de epifyten op Taiwan en slechts weinig studies betroffen de ecofysiologie van epifyten, in het bijzonder in samenhang met klimaatverandering en de veronderstelde bijhorende veranderingen in CO2 aanbod en zonneschijn. Daardoor was het niet mogelijk om een goed onderbouwde voorspelling te doen over de invloed van klimaatverandering op de epifyten van Taiwan.

Taiwan is een eiland in Oost Azië (21°45'–25°56’N en 119°18'–124°34'O) met een oppervlakte van 36,000 km2. De topografie van het eiland wordt gedomineerd door een longitudinale centrale bergketen en ongeveer 70% van het eiland is bergachtig (1000-3952 m). De jaarlijkse neerslag varieert tussen 1000 en 6000 mm, afhankelijk van de overheersende windrichting.

Dit onderzoek beoogt inzicht te verkrijgen in de invloed van klimaatverandering op Taiwanese epifyten. In het bijzonder worden de volgende hypotheses getest: 1) de samenstelling van de epifytische flora is vergelijkbaar met die in andere tropische gebieden; 2) de epifytische flora bestaat uit een mengeling van de soorten in nabijgelegen gebieden en wordt beïnvloed door de richting van de aanlandige winden; 3) in de bergen wordt de hoogste diversiteit aan epifyten op een middenhoogte gevonden, hetgeen beter verklaard wordt milieufactoren dan door een neutraal verbreidingsmodel van soorten langs de helling; 4) de evolutie van Crassulacean Acid Metabolism (CAM) in epifyten van vochtige bossen werd aangedreven door de beschikbaarheid van CO2; 5) de fotosynthetische capaciteit in de varen Asplenium nidus is groter aan de zonzijde van het blad dan aan de schaduwzijde; 6) de wijdverbreide epifytische varen Asplenium antiquum vertoont intraspecifieke variatie waardoor individuele planten verschillend reageren op klimaatverandering; 7) de verbreiding van epifyten is gecorreleerd met die van bosformaties; 8) bepaalde epifyten en bosformaties zijn relatief gevoelig voor klimaatverandering.

Teneinde de verschillende hypotheses te testen zijn zowel beschrijvende als experimentele (laboratorium- en veldstudies) en modelmatige onderzoeken uitgevoerd. Een op herbariumcollecties gebaseerde beschrijvende studie gaf inzicht in de floristische samenstelling van de epifytische vaatplanten en hun verbreiding en diversiteitpatronen (hypothese 1-3, hoofdstuk 2,3). Laboratorium- en veldexperimenten gaven inzicht in de veronderstelde evolutie van CAM naar aanleiding van de dagelijkse schommeling in CO2 (Hoya carnosa) en in

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SAMENVATTING de fotosynthetische capaciteit van varenbladeren (Asplenium antiquum) onder gesimuleerde omstandigheden van klimaatverandering (hypothese 4,5, hoofdstuk 4,5). Een veldexperiment werd ook ingezet om de mogelijke biologische aanpassingen van lokale populaties van de wijdverbreide varen Asplenium antiquum te onderzoeken onder diverse gesimuleerde omstandigheden van klimaatverandering (hypothese 6, hoofdstuk 6). Tenslotte is een modelmatige aanpak gekozen om de verbreidingspatronen van epifyten te analyseren (hypothese 3, hoofdstuk 3) en om de potentiële impact van klimaatverandering op bosformaties en hun epifyten te kunnen voorspellen (hypothese 7,8, hoofdstuk 7).

Hoofdstuk 2. Samenstelling en fytogeografie van de epifytische flora (Composition and phytogeography of the epiphyte flora)

Door middel van raadpleging van herbariumcollecties, literatuuronderzoek en veldobservaties is een checklist van epifytische vaatplanten opgesteld met in totaal 336 soorten in 105 genera en 24 families. Het Epifyten- Quotiënt (i.e. het aandeel van het aantal soorten epifyten in de flora) bedroeg slechts 8%. Vermoedelijk hebben de frequente tropische stormen (tyfoons) bijgedragen aan de relatief geringe diversiteit aan epifyten op Taiwan. Evenzo als in andere tropische gebieden wordt de epifytische flora gedomineerd door slechts enkele groepen planten, in het bijzonder varens (171 soorten) en orchideeën (120 soorten). De bijdrage van het aantal endemische soorten is hoog (21.3%), waarvan de helft orchideeën. De fytogeografie van de flora laat een vergelijkbare affiniteit met de flora’s van Maleisië, Oost Azië en de Indonesische archipel zien, maar de epifytische orchideeën hadden veel soorten gemeen met de flora van Indo-China wat vermoedelijk een gevolg is van de dominerende windrichting vanuit die streek.

Hoofdstuk 3. Verklarende factoren voor de verbreidingspatronen van epifyten (Epiphyte distribution pattern and explanatory factors)

Met behulp van de analyse van 39,084 ongedupliceerde botanische collecties en waarnemingen is de verbreiding van 300 soorten epifyten in de bergen gedocumenteerd. Een piek in het aantal soorten op een hoogte van 500 tot 1500 m kon niet verklaard worden door het neutrale ‘mid-domain effect’, hetgeen doet vermoeden dat vooral milieuvariabelen de verbreiding van soorten bepalen. De potentiële verbreiding van iedere soort is daarnaast gemoduleerd met behulp van verbreidingsmodellen (MaxEnt). De resultaten van de modellen bevestigden de piek in diversiteit op de middenhoogte en identificeerde twee gebieden met een uitzonderlijk hoge diversiteit. Deze epifyten ‘hotspots’ danken hun bestaan waarschijnlijk aan de optredende windrichting. Een correspondentie-analyse liet zien dat de verbreiding van epifyten vooral bepaald wordt door de factoren temperatuur (hoogte) en neerslag, maar dat taxonomische groepen verschillen in hun voorkeur op de thermische hoogtegradiënt. Zo kwamen

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SAMENVATTING hemiepifyten vooral in het laagland voor terwijl varens een voorkeur voor grotere hoogtes hadden. In tegenstelling tot de verwachting bij het optreden van het Rapoport effect liet de correspondentie-analyse ook zien dat de mate van thermische specialisatie van de soorten toenam met de hoogte waardoor soorten hoog in de bergen mogelijk meer gevoelig zijn voor opwarming van de aarde dan laaglandsoorten. Een partiële correspondentie-analyse van de invloed van tyfoons op de verbreiding van epifyten waarbij het effect van alle overige variabelen werd geëlimineerd liet tenslotte zien dat tyfoons inderdaad de verbreiding van epifyten significant beïnvloeden.

Hoofdstuk 4. De koppeling tussen de evolutie van CAM in de epifyt Hoya carnosa en de beschikbaarheid van CO2 (CO2 availability and the evolution of CAM in the epiphyte Hoya carnosa)

De ophoping van zuren en de verhouding van stabiele isotopen in het blad werden geanalyseerd van twintig Hoya carnosa CAM planten die verzameld werden onder twee categorieën van veldomstandigheden. Tien planten groeiden op bomen in een ongestoord dicht bos met een gesloten kronendak en tien planten waren afkomstig uit een meer open bos. -1 In het gesloten bos was de CO2 concentratie ’s nachts significant hoger (40-60 µmol mol ) dan overdag en gedurende de nacht was de concentratie in het gesloten bos ook hoger dan in het open bos wat toegeschreven kan worden aan de hogere ademhaling van de bomen in het dichte bos. Desalniettemin, was de verhouding van stabiele isotopen in de Hoya carnosa planten niet substantieel lager dan in veel andere CAM planten wat suggereert dat de gedurende de nacht extra hoeveelheid vrijkomende CO2 geen belangrijke CO2 bron was voor deze CAM planten. Bovendien lieten laboratorium experimenten zien dat Hoya carnosa planten overdag een aanzienlijke hoeveelheid CO2 opnemen wat de koolstof isotoopwaarden van deze soort zelfs zou moeten verlagen. Het ziet er dus naar uit, dat de ademhaling van de gastbomen niet fundamenteel bijdraagt aan de CO2 huishouding van de epifyten in het kronendak en daarmee wordt de hypothese onderbouwd dat in de evolutie van epifyten CAM is ontstaan om waterverlies te beperken en niet als reactie op de dagelijkse schommelingen in CO2 concentratie.

Hoofdstuk 5. Plasticiteit in het fotosynthetische vermogen van de epifytische varen Asplenium nidus (Plasticity of photosynthetic capacity in the epiphytic fern Asplenium nidus)

Het verschil in fotosynthetische vermogen tussen de zon- en schaduwzijde van epifytische varenbladeren werd met elkaar vergeleken door in situ de CO2 gasuitwisseling te meten. Bladeren van Asplenium nidus vormen een rozet en afhankelijk van de positie van de bladeren in

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SAMENVATTING het rozet werden verticale-, horizontale- en bladeren onder een hoek, met elkaar vergeleken. De drie bladtypen komen overeen met verschillen in bloostelling aan de zon. De resultaten van de metingen gaven aan dat de intensiteit van de fotosynthese hoger was indien de kant van het blad die normaal meer zonlicht ontvangt in het experiment belicht werd, met uitzondering van verticale bladeren. Omdat de stomatale weerstand en de daaraan gekoppelde transpiratiesnelheden gelijk waren werd de hogere CO2 opnamesnelheid toegeschreven aan een groter biochemisch fotosynthetisch vermogen. Het onderzoek liet zien dat onder verschillende milieuomstandigheden epifyten beschikken over fysiologische plasticiteit.

Hoofdstuk 6. Adaptatie van de wijdverbreide epifytische varen Asplenium antiquum aan gesimuleerde omstandigheden van klimaatverandering. (Adaptation of a widespread epiphytic fern, Asplenium antiquum, to simulated climate change)

Om het vermogen tot adaptatie van de wijdverbreide epifytische varen Asplenium antiquum aan gesimuleerde omstandigheden van klimaatverandering te bestuderen werd een tweejarig veldexperiment uitgevoerd waarbij kiemplanten wederkerig uitgeplant werden op drie locaties langs een hoogtegradiënt. De resultaten lieten zien dat de drie locaties, op 600m, 1100m en 1950 m hoogte, een sterke invloed hadden op zowel de groei als de mortaliteit van de jonge Asplenium antiquum planten. Op de hoge locatie had de lokale populatie een significant lagere mortaliteit dan de twee andere populaties waarmee de lokale planten aantoonbaar beter aangepast waren aan het meer extreme klimaat ter plaatse. Deze resultaten suggereren dat intraspecifieke genetische variatie meegewogen moet worden bij de evaluatie van het potentiële effect van klimaatverandering op soorten.

Hoofdstuk 7. Een model van het effect van klimaatverandering op bossen en hun epifyten. (Modelling climate change impacts on forests and associated epiphyte)

Hiërarchische soort-distributiemodellen (SDM’s) werden ontwikkeld om het effect van klimaatverandering op bossen en 237 soorten epifytische vaatplanten op Taiwan te kunnen voorspellen. Om de nauwkeurigheid en het realisme van de het SDM’s te vergroten werd een nieuwe manier van aanpak toegepast bij de constructie van de modellen waarbij rekening gehouden werd met 1) de beperkingen aan de ruimtelijke verspreiding van de soorten, de resistentie van bomen volgend op een verandering van het klimaat, met niet klimaat gerelateerde factoren, en 2) met de biotische interactie tussen epifyten en hun waardbomen. De gemodelleerde resultaten deden vermoeden dat de verbreiding van epifyten sterk afhankelijk was van het type bos. De jaargemiddelden van de klimaatvariabelen en de bijhorende variaties

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SAMENVATTING hadden evenveel invloed op de gemodelleerde verbreiding van de soorten en niet aan het klimaat gerelateerde factoren behielden over het algemeen hun invloed bij veranderende klimaatomstandigheden. Ons model gaf ook aan dat sommige bosformaties (e.g. Cypress and Picea bossen) en sommige temperatuur- of droogtegevoelige soorten relatief kwetsbaar waren voor de voorspelde scenario’s van klimaatverandering op het eiland.

Samenvattend heeft het beschrijvend onderzoek aan de epifyten laten zien dat de Taiwanese epifytische flora niet uitzonderlijk is voor een tropisch eiland. Zo is ook op Taiwan de diversiteit aan soorten relatief gering in vergelijking tot het vaste land, weliswaar met veel endemische soorten, en zijn de dominante groepen, zoals varens en orchideeën, vergelijkbaar met wat we kennen van andere tropische eilanden. De relatief lage diversiteit, zowel absoluut als in verhouding tot de gehele flora, kan vermoedelijk in ieder geval deels toegeschreven worden aan de veelvuldig optredende verwoestende tyfoons op Taiwan. De modellen lieten zien dat de verbreiding van de soorten in de bergen, en de daaraan gekoppelde verschillen in diversiteit, vooral bepaald werd door milieufactoren en in mindere mate verklaard kon worden door een ruimtelijk beperkt neutraal model. Het laboratoriumonderzoek liet evenwel ook zien dat epifyten een aanzienlijk fysiologisch aanpassingsvermogen ten toon kunnen spreiden aan de verschillende milieuomstandigheden in het kronendak van het bos. Een veldexperiment gaf bovendien aan dat een wijdverbreide soort intraspecifieke adaptatie vertoont tussen populaties van verschillende hoogten. Om de invloed van klimaatverandering op de epifytische biodiversiteit goed te kunnen voorspellen is informatie over de mate van fysiologische plasticiteit en de mate van genetische adaptatie van de soorten essentieel.

De Cypress en Picea bossen op een middenhoogte in de bergen, tenslotte, herbergen een groot aantal specialistische epifyten en verdienen daarmee de bijzondere aandacht van natuurbeschermers.

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I write because I don’t know what I think until I read what I have to say.

–Flannery O’Connor

174

ACKNOWLEDGEMENTS

It seems unreal to me at this moment when I finish this book filled with gratefulness. For a time, I even wondered whether being a scientist would be a suitable profession for me. Therefore, I have to express my sincere gratitude to my promoters, Jan, Gerard, Wil and Geert, for your valuable advice and great support of my work, and training me to think orderly and logically. Although most of the time I stayed in Taiwan’s forests doing my work, the spatial distance has not been a gap between us at all. Especially for Jan, without your guidance and endless patience, I would not have been able to make it. Thanks! And I do enjoy your incredible stories about epiphyte research in the field. I also own special thanks to Niels Raes and Craig Martin, for your inspiration and long term influence (in a good way) from the very beginning of my academic career.

I appreciate the Taiwan forestry research institute (TFRI) for giving me great freedom to do my own research. The laboratory support of spore germination provided by Chiou, W.‐L. (邱文良) and Huang, Y.‐M. (黃耀謀 ) is gratefully acknowledged. My special thanks go to Yu S.‐ K.(余勝焜), Chung S.‐W. (鐘詩文 ), Lu P.‐F. (呂碧鳳), Chang Y.‐H. (張藝翰 ), and Chen, C.‐H. (陳志輝) for sharing their observations on Taiwanese epiphytes in the field, and to Su, D.‐J. (蘇德忠) and Yu, S.‐Y. (余偲嫣) for their assistance with the tiring fieldwork. Special thanks are extended to Lin, T.‐C. (林登秋 ), Lin, K.‐C. (林國銓), Lin, S.‐H. (林信輝), Zhuang, Z.‐H. (莊志弘) and Tung, G.‐S. (董景生) for their help with several aspects of this study.

I would like to thank Lin, S.‐H. (林淑華) (Academia Sinica) and Lee, P.‐F. (李培芬) (Spatial Ecology Laboratory) as well as Chiu, C.‐R. (邱祈榮) (Lab natural resource investigation & analysis) at National Taiwan University for providing climatic data layers and forest occurrences. I am grateful for impressive herbarium collections kindly provided by the herbarium of the Taiwan forestry research institute (TAIF), the herbarium of the biodiversity research center, academia sinica, Taipei (HAST), the herbarium of national Taiwan university (TAI), the national museum of natural science herbarium (TNM) and the Taiwan endemic species research institute (TESRI).

To Brian, my life partner, thank you for tolerating my capricious mood, sometimes“weirdity” during this period of time, and being very frank when I need your opinions. I am proud to present this book to you now. 最後，僅以本書獻給我摯愛的父母與家人，謝謝你們!!

嘉君 exuxvvt `tçA ECDF

Rebecca C.‐C. Hsu (徐嘉君) was born on Jan. 11th, 1974 in HsinChu, Taiwan. In 1996, she earned a Bachelor degree in Industrial Design at National Cheng Kung University, yet also took courses in Biology and was supervised by Prof. Kuo, Chang‐Sheng (郭長生). The same year she continued studying Botany at National Taiwan University. Under supervision of Prof. Kuo, Chen‐Meng (郭城孟) and Dr. Hong, Fu‐Wen (洪富文) from Taiwan Forestry Research Institute (TFRI), she started the study on epiphyte biomass and nutrient contents in the Fushan experimental forest, and obtained her MSc. degree in 1998. Since then, she worked in TFRI and at the Taiwan Forestry Bureau, assisting research projects and forest management affairs. She also worked with a visiting scholar, Prof. dr. Craig Martin, and together they published several ecophysiological studies on vascular epiphytes in FuShan. In 2005, she received a scholarship from the Nation Science Council to study Sustainability and Biodiversity at Leiden University for a second MSc degree. She was supervised by Dr. Niels Raes and Dr. Wil Tamis and finished two research projects concerning the genus Cymbidium (Orchidaceae) and the distribution of Taiwanese vascular epiphytes, using computer modelling tools. During this period, she began to write a PhD proposal, which was inspired by an El Niño event during her research in FuShan. After graduating from Leiden University in 2007, she came back working in TFRI and accomplished the present doctoral thesis. For her publications, please visit the website: http://rebecca.ecogarden.tw/. ISBN: 978-94-91407-12-3

Institute for Biodiversity Institute of Environmental Science and Ecosystem Dynamics KRONENDAK