Local and regional determinants of vascular ... - BES journal - Wiley

Journal of Ecology 2016, 104, 841–849

doi: 10.1111/1365-2745.12563

Local and regional determinants of vascular epiphyte mortality in the Andean mountains of Colombia pez-Rios3 and Alvaro Duque4* Daniel Zuleta1,2, Ana M. Benavides1, Victor Lo n para Investigaciones Biolo gicas – CIB, Medellın, Colombia; 2Posgrado en Bosques y Conservacio n Corporacio 3 Ambiental, Universidad Nacional de Colombia Sede Medellın, Medellın, Colombia; Escuela de Estadıstica, Universidad Nacional de Colombia Sede Medellın, Medellın, Colombia; and 4Departamento de Ciencias Forestales, Universidad Nacional de Colombia Sede Medellın, Medellın, Colombia 1

Summary 1. We present the first large-scale assessment of vascular epiphyte mortality in the neotropics. Our goals were to explore the primary types of vascular epiphyte death and to identify local and regional determinants of epiphyte mortality in natural forests located 60 to 2900 m a.s.l. in the Colombian Andes. 2. Based on two consecutive annual surveys, we followed the fate of 4247 epiphytes to estimate the epiphyte mortality rate on 116 host trees at nine sites. A logistic regression analysis for proportional data with a binomial distribution of the error was applied to determine the probability of epiphyte death in relation to local and regional explanatory variables. 3. The overall epiphyte mortality rate was 7.5 1.1% year1 (mean standard error). Nonmechanical factors, such as desiccation, accounted for a mortality rate of 1.9 0.3% year1. Mechanical factors, such as falling branches, accounted for a mortality rate of 5.6 1.1% year1. According to generalized linear modelling analyses, both local and regional factors played key roles in determining epiphyte mortality. The actual evapotranspiration (regional factor) and the mean epiphyte attachment height (local factor) were both consistently positively associated with the probability of epiphyte death. Additional variables identified as possible determinants of the epiphyte mortality were the temperature seasonality, annual temperature range, the height and number of branches of the tree and the abundance of large trees (DBH ≥10 cm). 4. Synthesis. The recorded high mortality rate indicates that natural epiphyte assemblages must be highly dynamic to avoid local extinction of species. Our study identifies actual evapotranspiration as an important driver of epiphyte mortality, and we highlight its importance in determining the fate tropical epiphyte communities may experience if evapotranspiration increases due to climate change. We hope our study addresses the paucity of research on non-tree growth forms, typically ignored in vegetation dynamics, and encourages their inclusion in future studies that investigate the function of tropical ecosystems. Key-words: branchfall, epiphytic survival, evapotranspiration, microhabitat heterogeneity, plant population and community dynamics, spatial scale, tropical forest dynamics

Introduction In tropical humid forests, vascular epiphytes (i.e. non-parasitic plants that use other plants as support; Benzing 1990) can represent up to 50% of the total local vascular species richness (Gentry & Dodson 1987). However, the underlying mechanisms controlling species assemblages of vascular epiphytes (hereafter simply referred to as epiphytes) are largely *Correspondence author: E-mails: [email protected] or ajduque @unal.edu.co

unknown, which contrasts with the accumulated knowledge on the dynamics of other growth forms, such as trees (e.g. Phillips et al. 1998, 2009; Condit et al. 2004). For example, biotic interactions, such as plant competition, have been shown to play a key role in shaping tree dynamics (Peters 2003; Fort & Inchausti 2013), but for epiphyte assemblages, mostly low plant densities suggest that competition is markedly low (Benzing 1990). Since the mean annual mortality rate of epiphytes can be up to three times (10.8% year1; Laube & Zotz 2006) the mortality rate of trees (1–3%; Condit et al. 2006), the latter may be considered a poor indicator of

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society

842 D. Zuleta et al. epiphyte dynamics (Mendieta-Leiva & Zotz 2015). Hence, improving our understanding on some basic demographic properties of vascular epiphyte assemblages, such as mortality, will help unravelling the role played by this growth form on forest functioning. Epiphyte mortality caused by climatic factors (e.g. water deficit) or biological interactions (e.g. pests or pathogens) occurs via physiological constraints that then lead to plant desiccation (Zotz & Hietz 2001; Winkler, H€ulber & Hietz 2005). However, in tropical forests, the predominant cause of epiphyte death is disturbance, which we define as any natural event that induces changes in forest structure or loss of biomass (Huston 1994). Indeed, most of the total epiphyte mortality has been attributed to mechanical factors, such as branchfall (Hietz 1997; Sarmento Cabral et al. 2015), rather than to non-mechanical factors, such as water deficit. Epiphyte differs from other plant growth forms (i.e. trees) in many respects, and providing insight into the main causes of their mortality will contribute to the mechanistic understanding behind the structure and composition of tropical plant communities (Mondragon 2011). The establishment and survival of epiphytes depend on factors that operate at different spatial scales. At the local scale, epiphyte dynamics are influenced largely by forest structure. As such, microclimatic variation given by the vertical gradient in forest canopies creates a physical mosaic that fine-tunes niche partitioning of humidity, light and temperature (Johansson 1974; Benzing 1995; Kr€omer, Kessler & Gradstein 2007; Woods, Cardelus & DeWalt 2015). Epiphytes situated in tree crowns could experience higher mortality due to exposure to higher temperatures, radiation, wind intensity, aridity and substrate instability (e.g. branchfall) compared with species established on the bole or on the understorey (Chazdon & Fetcher 1984; Parker 1995; Freiberg 1997; Hietz 1997; Werner 2011). At the regional scale, macroclimatic variation generates the main environmental filter that defines epiphyte species composition and patterns in distribution (Gentry & Dodson 1987; Wolf 1994; Kreft et al. 2004). Although there is some information on epiphyte mortality at a local scale (Hietz 1997; Laube & Zotz 2006), we lack quantitative assessments that aim to identify the main causes of epiphyte mortality at a regional scale. The scale-dependent nature of these processes asks for a scale-dependent approach to achieve a better understanding of the dynamics of this important component of tropical forests. Here, we present the first assessment of epiphyte mortality conducted on a large scale in the tropical Andes Mountains and surrounding lowlands. Using two consecutive epiphyte surveys performed between 2013 and 2014 at nine different sites along a complex environmental elevational gradient in north-west Colombia, we aimed to quantify the extent to which local and regional factors determine the mortality of vascular epiphytes. Our main research questions were as follows: 1) What proportion of total mortality can be attributed to mechanical or non-mechanical factors? 2) What are the main local and regional environmental determinants of the observed epiphyte mortality rates? This study attempts to

improve knowledge regarding the dynamics of this growth form, that is potentially highly threatened as a consequence of global change (Duque et al. 2014).

Materials and methods STUDY REGION

The study area was located in the north-west region of Colombia between 5°500 –8°610 N and 74°610 –77°330 W (Fig. 1). The topography and geology in the region are highly variable because of the presence of two mountain ranges that influence the patterns of drainage, rainfall and soil fertility at local scales (Instituto Geografico Agustın Codazzi - IGAC 2007). We registered epiphyte mortality at nine sites in permanent 1-ha tree plots (100 m 9 100 m). These plots were distributed across a large geographical area in the Andes (64 000 km2), mostly in the province of Antioquia (see Duque, Stevenson & Feeley 2015). The plot locations span an elevational gradient from 60 to 2900 m a.s.l. and the annual precipitation ranges from 2220 to ca. 4270 mm year1 (see Table S1 in Supporting Information for details). In the entire province of Antioquia, the current forest cover only accounts for approximately 30% of the original vegetation (Duque et al. 2014).

EPIPHYTE SAMPLING AND MORTALITY ASSESSMENT

To assess mortality rates, vascular epiphytes were tallied twice (2013–2014). At each site, the minimum time between censuses was 12 months. To sample the epiphytes, we adapted the SVERA method proposed by Wolf, Gradstein & Nadkarni (2009), which aims to assess epiphyte richness and abundance. In each plot, we haphazardly selected 35 host trees distributed in the following six size classes: 10 trees with a diameter at breast height (DBH) > 30 cm and 25 trees in five classes with a smaller size (5–10, 10.1–15, 15.1–20, 20.1–25 and

Fig. 1. Location of the nine sites surveyed (black triangles) in the north-west Andes of Colombia.

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology, 104, 841–849

Determinants of vascular epiphyte mortality 843 25.1–30 cm DBH). We included host trees with smooth, hard or sloughing bark. For each host tree, we recorded the geographical position, DBH, tree height (HTree) and the number of branches with an estimated diameter greater than or equal to 5 cm at the branching point (BranchNum). For each host tree, all vascular epiphytes (i.e. epiphytes, nomadic vines, hemiepiphytes, facultative epiphytes and accidental epiphytes; Moffett 2000; Zotz 2013) were mapped using binoculars, registered and in most cases, photographed. In some cases, host trees were climbed and photographs of the epiphytes were taken in order to assign a taxonomic classification based on collections made in the surrounding trees. The use of binoculars from the ground may underestimate total epiphyte species abundance, richness and underrepresent upper canopy epiphytes (Flores-Palacios & Garcıa-Franco 2001; Gradstein et al. 2003). Therefore, our study is likely to have a bias towards mid-canopy epiphytes. Epiphyte individuals were defined as all independent stems or packed groups of conspecific plants that were spatially separated and distinguishable from each other (Sanford 1968). Nonetheless, spatially separated stems or plants suspected to belong to the same genet were counted as different individuals. Epiphytes with climbing habits (e.g. some ferns, aroids and gesneriads) were counted as separated individuals if their rhizomes and stems were not connected. In cases of densely packed patches of plants or branches and trunks difficult to monitor with binoculars, zoomed-in photographs were used to determine the presence or absence of epiphyte individuals. 57.6% of the individuals were identified to the species level, 38.3% at the genus level, 2.4% at the family level and 1.6% were unidentified. Voucher specimens are deposited in the Herbarium of the University of Antioquia. For each epiphyte individual, we recorded its azimuth, the height above-ground at the attachment site, the estimated size and the i-th branch of the tree on which it was found. The height above-ground was measured to the nearest centimetre using telescopic fibreglass poles (Hastings Measuring Sticks 3JF-108823) 15 m in length. When the location of the epiphyte exceeded 15 m, the remaining height was estimated and added to the 15 m pole, which was used as a reference. The size of the plant was defined as the length of the longest leaf for epiphytes and as the length of the stem for nomadic vines and hemiepiphytes. We assessed the relationship between estimated size (binocular observation) and measured size for 246 individuals (adjusted R2 = 0.75; d.f. = 244; P < 0.0001; see Fig. S1 in Supporting Information). We excluded epiphytes smaller than 5 cm, which in many cases were seedlings because of the difficulty to monitor them from the ground, but three orchid species (two Stelis and Eurystyles cotyledon) were included because even adult plants do not surpass this size. We distinguished mechanical or non-mechanical causes of mortality. Mechanically induced mortality included falling branches or entire plants, detached bark or factors such as the effects of animals or wind. Fallen individuals were considered dead because of their low probability of surviving on the forest floor (Matelson, Nadkarni & Longino 1993; Mondragon & Ticktin 2011). Mortality caused by non-mechanical factors was assigned to plants that perished attached in situ because of reasons other than mechanical factors. In most cases, individuals lacking photosynthetically active tissue characterized mortality due to non-mechanical factors.

LOCAL AND REGIONAL DETERMINANTS OF EPIPHYTE MORTALITY

In each 1 ha plot, all of the shrubs, trees, palms and tree ferns with a DBH ≥10 cm were mapped, tagged and measured. All individuals

with a DBH between 1 and 10 cm were counted in a 40 9 40 m subplot located near the centre of each plot (Duque, Stevenson & Feeley 2015). Since water and light distribution across forest strata is determined by forest structure (Allen et al. 1972; Parker 1995), we used the structural variability as a surrogate of microclimate at a local scale. The structural variables that were considered possible determinants of epiphyte mortality were the following: basal area of individuals with a DBH ≥5 cm (AB); number of trees with DBH ≥10 cm (Ind10); number of understorey individuals (5 ≤ DBH < 10 cm); and maximum height (Hmax), calculated as the average of the 10 largest trees in each plot. Tree height was measured for roughly 40% of individuals within each plot. For individuals with heights lower than 15 m, we used a fibreglass telescopic pole; otherwise, a laser rangefinder hypsometer (Nikon 550) was employed (see Duque, Stevenson & Feeley 2015). At the individual host tree level, we also included the following as likely explanatory factors: HTree, BranchNum, mean epiphyte attachment height (MEAH) and estimated mean size of epiphytes (MSP) (see Table S1). Both individual tree and plot scale variables were considered as local-scale explanatory factors. We used the main climatic variables estimated at each site at a spatial resolution of 30 arc-s (c. 1 9 1-km resolution) as likely regional determinants of epiphyte mortality. The variables employed were as follows: actual evapotranspiration (AET); mean diurnal temperature range [MDT: mean of the monthly range (maximum temperature– minimum temperature)]; temperature seasonality (TS: standard deviation 9 100); annual temperature range (ATR); annual precipitation (AP); precipitation in the driest month (PDM); and precipitation seasonality (PS: coefficient of variation). AET was obtained from the Global Soil Water Balance Geospatial Database (http://www.cgiarcsi.org; Trabucco & Zomer 2010) and is referred to as the loss of water from the soil by evaporation and transpiration. All other climatic variables were downloaded from the WorldClim Database (http://www.worldclim.org; Hijmans et al. 2005) (see Table S1).

DATA ANALYSIS

In order to improve the accuracy of the results, and to avoid a bias due to a small sample size, we applied two filters to each host tree before analysing epiphyte mortality. First, during the second survey, we classified sections of branches and trunks carrying epiphytes as either reliable or non-reliable. Reliable sections were those with mapped locations of all plants that could be traced from the first survey (i.e. individuals were not concealed by other branches, overgrown by epiphytes and whose mapped locations did not greatly differ between censuses). Only those sections classified as reliable were used for the analysis. After selecting reliable sections, we applied a second filter by including only those host trees that had 10 or more epiphyte individuals to obtain a sample size that was as large as possible (Fiske, Bruna & Bolker 2008). The application of filters allowed us to reduce data overdispersion and improve both the accuracy and precision of the statistical model. After applying these two filters, 116 out of 315 host trees were finally selected to analyse epiphyte mortality. The different incidence of epiphyte abundance and occupancy between lowland and highland forests resulted in imbalanced sample sizes in the final data set (see Table 1). We estimated the total mortality rate (mechanical and non-mechanical factors together), the mortality due to mechanical factors and the mortality resulting from non-mechanical factors at the host tree level. The mortality rate (m) was estimated using the equation recommended by Sheil, Burslem & Alder (1995) over relatively short periods (~1 year) defined as: m (% year1) = 1-(N1/N0)(1/t), where N0 and N1


844 D. Zuleta et al. Table 1. Total mortality rate, mortality due to non-mechanical factors and mortality resulting from non-mechanical factors for vascular epiphytes on 116 sampled host trees at nine sites in the Colombian Andes

Site name

Total mortality rate (% year1)

Caucasia El Bagre Segovia Amalfi Anorı Valdivia Angel opolis Jardın Belmira Mean SE

3.9 9.2 8.8 13.0 6.7 8.4 15.6 6.7 4.8 7.5

5.5

8.2 11.7 6.8 19.7 16.6 7.2 4.0 1.1

Non-mechanical mortality rate (% year1) 3.9 0.0 1.4 5.4 2.8 0.6 2.62 2.78 1.46 1.9

5.5

3.0 9.4 3.6 1.6 3.88 4.19 1.96 0.3a

Mechanical factors mortality rate (% year1) 0.0 9.2 7.5 7.6 3.9 7.8 13.0 3.9 3.3 5.6

0.0

9.2 13.1 5.2 19.8 16.3 4.6 3.8 1.1b

Total number of epiphytes per site

Number of host trees with ≥10 epiphytes

23 10 97 34 731 645 282 555 1870 472 188

2 1 5 3 26 25 10 11 33 12 4

Elevation (m a.s.l.) 62 67 769 1006 1783 2080 2183 2525 2887

Superscript lower case letters indicate significant differences (P < 0.05). The sites are ordered from lowest (~60 m a.s.l.) to highest elevation (~2900 m a.s.l.). SE, standard error.

are the number of epiphyte individuals found in the initial and final survey, respectively, and t is the average annualized time between the two surveys. To answer the first research question, the difference between the mortality caused by mechanical and non-mechanical factors was evaluated using the Mann–Whitney test (a = 0.05). To investigate the local and regional determinants of the epiphyte mortality rates, a generalized linear model (GLM) was constructed. A logistic regression analysis for proportional data with a binomial distribution of the error was applied to determine whether the probability of death was related to the explanatory variables. We fitted the same model for total mortality, mortality due to mechanical factors and mortality caused by non-mechanical factors. Because of the greater number of zeros than ones associated with the probability of death (i.e. many host trees with zero or low rates of epiphyte mortality), we used the complementary log–log link function (clog–log) as suggested by Zuur et al. (2009). To avoid obtaining spurious results, we assessed outliers, homogeneity, normality, collinearity, interactions and the independence of covariates and data following Zuur, Ieno & Elphick (2010). For instance, to obtain a set of explanatory variables without collinearity, we calculated the variance inflation factor (VIF) by removing one variable at a time and recalculating the VIF values. This process was repeated until variables with VIF values less than three were attained (Zuur et al. 2009). In addition, we considered second-order interactions between all of the selected covariates and then performed variable selection again, based on the collinearity. Given the high collinearity between the variables that were initially considered to build the final models, we based all analyses on only four climatic variables (MDT, TS, ATR and AET), one variable related to forest structure (Ind10), four host tree variables (MEAH, MSP, HTree and BranchNum) and the interaction between MSP and BranchNum. Therefore, the initial GLM to answer the second research question regarding the determinants of mortality was as follows: Logit (Pi) = b0 + b1 (MDT) + b2 (TS) + b3 (ATR) + b4 (AET) + b5 (Ind10) + b6 (MEAH) +b7 (MSP) + b8 (HTree) + b9 (BranchNum) + b10 [(MSP) 9 (BranchNum)] + e, where Pi is the probability of death in the i-th host tree, and b-values are the model parameters to be estimated. The most parsimonious model was selected using the backward stepwise model selection procedure based on the Akaike information criterion (AIC) (Crawley 2007). For model checking, deviance

residuals were used as is recommended by Pierce & Schafer (1986) for response variables with many zeros. One dead host tree was removed from the analyses because it was classified as highly influential in accordance with the Cook’s distance (larger than 1; Fox 2002). To analyse the effect of each significant explanatory variable that remained in the final model, we conducted a sensitivity analysis to predict the probability of death within the observed range of values for that particular variable while fixing the other explanatory variables at their average. Finally, we used semi-variograms as in the GEOR package (Diggle & Ribeiro 2007) to assess the spatial autocorrelation of the residuals in each model. All of the analyses were conducted using R 3.1.2 (R Core Team 2014).

Results MORTALITY PATTERNS

Among the 116 surveyed host trees, 4247 epiphyte individuals (distributed in 40 families, 105 genera and 389 morphospecies) were found on 654 branches and stem sections. In the second survey, we recorded 248 dead epiphytes equivalent to a regional annual mortality rate of 7.5 1.1% year1 (mean standard error; Table 1). We found no significant correlation between (log-transformed) elevation and total mortality (r = 0.21; P > 0.05), mortality caused by mechanical (r = 0.19; P > 0.05) and non-mechanical factors (r = 0.04; P > 0.05). The mean average mortality rate per host tree due to mechanical factors (5.6 1.1% year1) was significantly higher (Mann–Whitney: 8711; P < 0.001) than that due to nonmechanical factors (1.9 0.3% year1) (Table 1). The 248 dead epiphytes belonged to 23 of the 39 families recorded in the first census. Bromeliaceae (24.2%), Orchidaceae (15.3%), Polypodiaceae (14.9%), Araceae (13.7%) and Dryopteridaceae (10.5%) were the families with the highest percentages of dead individuals. At the (morpho) species level, the 248 dead individuals belonged to 124 of the 389 species found in the first census, 78 of which had a single dead individual. The species with the largest number of dead individuals was the grammitid fern Melpomene flabelliformis (11 dead individuals).


Determinants of vascular epiphyte mortality 845 DETERMINANTS OF EPIPHYTE MORTALITY

Both local and regional factors were found to play key roles in determining epiphyte mortality. Overall, actual evapotranspiration (regional factor) and the mean epiphyte attachment height (local factor) were positively correlated with the probability of death. This condition remained true for total mortality and that caused by mechanical and non-mechanical factors. Temperature seasonality was negatively associated with mortality due to non-mechanical factors, while the annual temperature range was negatively related to mortality resulting from mechanical factors. Host tree height and number of branches negatively affected the total mortality and the probability of death by non-mechanical factors, respectively. Similarly, the lower the number of individuals with DBH ≥ 10 cm, the higher the probability of epiphyte death because of mechanical factors (Table 2). We did not find any pattern of spatial autocorrelation in the residuals of the models (Fig. S2). According to the sensitivity analysis, actual evapotranspiration was the most important factor determining the probability of epiphyte death due to either mechanical or nonmechanical causes (Fig. 2).

Discussion PATTERNS OF EPIPHYTE MORTALITY

The overall epiphyte mortality rate observed in this study (7.5 1.1% year1), which represents the first survey conducted at a large scale in the neotropics, was similar to that reported in another long-term study investigating epiphytes at a local scale in the lowlands of Panama (10.8% year1; Laube & Zotz 2006). These findings indicate that to keep

apace with mortality, epiphyte assemblages inhabiting these tropical forests must have high turnover rates to avoid local extinction. Furthermore, the observed mean mortality rates in each of our study sites were quite heterogeneous and varied independently of elevation, which emphasizes the need to identify the mechanistic causes of epiphyte mortality that operate at fine spatial resolutions. In combination with studies at high resolutions, broad-scale assessments of recruitment and mortality will help to unravel the manner in which epiphyte assemblages are maintained. The mean annual epiphyte mortality we report is consistent with other studies dealing with vascular epiphytes (Hietz 1997; Laube & Zotz 2006) and is up to four times greater than those of typical growth forms, such as tropical trees (1.5%; see Condit et al. 2006). However, when we focus our analysis on the epiphyte mortality caused by non-mechanical factors, the observed mean mortality rate of 1.9 0.3% year1 did not differ at all from the 1.9 0.7% year1 mean mortality rate of adult trees reported in the same forests (Table S4 in Duque, Stevenson & Feeley 2015). Nonetheless, sampling issues like the exclusion of epiphytes with sizes lower than 5 cm should have reduced the observed mortality by masking the likely high mortality in these plant stages. Likewise, an underestimation of epiphyte mortality may have resulted from the difficulty of monitoring the higher and outermost branches (see Hietz 1997) where mortality is likely high because of harsh environmental conditions. Despite of being time-consuming and economically costly, improving the accuracy and sampling techniques employed to assess epiphyte mortality in tropical forests will surely help us to better quantify epiphyte mortality caused by non-mechanical factors as well as epiphyte turnover in tropical ecosystems.

Table 2. Summary of the logistic regression employed to model the probability of death of vascular epiphytes on 115 sampled host trees at nine sites in the Colombian Andes

Total mortality rate Intercept Temperature seasonality Actual evapotranspiration Mean epiphyte attachment height Tree height Mortality due to non-mechanical factors Intercept Temperature seasonality Actual evapotranspiration Mean epiphyte attachment height Number of branches on the host tree Mortality due to mechanical factors Intercept Annual temperature range Actual evapotranspiration Individuals with DBH ≥ 10 cm Mean epiphyte attachment height

Type of variable

Estimate

SE

z-value

P-value

NA Regional Regional Local Local

7.806 0.006 0.006 0.052 0.029

0.887 0.002 0.001 0.021 0.014

8.805 4.134 5.559 2.495 2.072

< 0.001*** < 0.001*** < 0.001*** 0.0126* 0.0383*


8.265 0.008 0.005 0.082 0.071

1.637 0.003 0.002 0.040 0.030

5.050 2.658 2.809 2.066 2.346

< 0.001*** 0.0079** 0.0050** 0.0388* 0.0190*


3.222 0.024 0.003 0.001 0.038

1.249 0.007 0.001 0.001 0.022

2.580 3.316 2.867 1.873 1.699

0.0099** < 0.001*** 0.0041** 0.0610 0.0892

NA, not applicable. *P < 0.05; **P < 0.01; ***P < 0.001. © 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology, 104, 841–849

846 D. Zuleta et al.

Probability of death

(a)

(b) 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0

0.5

0.3 0.2 0.1 0.0 0

20

40

60

80 100 120

Probability of death

(c)

−2

−1

0

1

2

(d) 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0

0.5

TS AET MEAH BranchNum

0.4 0.3 0.2 0.1 0.0 0

20

40

60

80 100 120

−2

−1

0

1

2

0

1

2

(f)

(e) Probability of death

TS AET MEAH HTree

0.4

0.5 0.4 0.3 0.2 0.1 0.0

0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0

20

40

60

80 100 120

Final variables on model

ATR AET Ind10 MEAH

−2

−1

Standardized values

Although non-mechanical factors were responsible for a good portion of the total mortality of epiphytes in these forests, disturbance was the principal cause of epiphyte mortality (see Table 1). In fact, external and indirect causes of mortality, such as branchfall and other mechanical factors, triggered most of the mortality we observed (5.6 1.1% year1). Branchfall could constrain epiphyte demography by increasing mortality (Sarmento Cabral et al. 2015), and even lead to negative population balances of many species (Hietz 1997; Winkler, H€ulber & Hietz 2007). Thus, the persistence of epiphyte communities would require species to shift recruitment towards individuals with shorter life cycles and rapid maturation (Hietz, Ausserer & Schindler 2002; Benavides, Wolf & Duivenvoorden 2013; Sarmento Cabral et al. 2015). Yet, most vascular epiphyte species have long life cycles, which can constrain faster recruitment, the capability to colonize new substrates and the likelihood of adapting to global change (Benzing 1998). As a result, it is possible for species with long life cycles and slow reproductive maturation to become locally extinct in frequent-disturbance scenarios. LOCAL AND REGIONAL DETERMINANTS OF EPIPHYTE MORTALITY

At the local scale, the mean epiphyte attachment height was a significant and systematic factor that explained epiphyte

Fig. 2. Final models and the sensitivity analysis according to the selected explanatory variables in the logistic regressions. The panels on the left present curves show the estimated probability of death in 115 host trees (black points) as a function of significant variables for total mortality (a), mortality caused by non-mechanical (c) and mechanical factors (e). Shaded areas around the lines show the 95% confidence intervals. The panels on the right show the sensitivity analysis of the explanatory variables for total mortality (b), mortality caused by nonmechanical (d) and mechanical factors (f). Curves show the probability of death as a function of the standardized values for each explanatory variable when other significant variables were fixed at their average.

mortality (Table 2; Fig. 2). Since microclimate has been shown to vary in relation to the size of host trees (Woods, Cardel us & DeWalt 2015), epiphyte attachment height can be assumed as a surrogate for microclimatic variation. Our findings show that, on average, epiphytes located in higher strata are at a greater risk of dying than those located in the lower compartments of the forest (Allen et al. 1972; Parker 1995; Kr€ omer, Kessler & Gradstein 2007). However, in the most exposed and less environmentally constant habitats, such as the outermost branches and crowns, the most xerotolerant epiphytes (i.e. many bromeliads and orchids) may exhibit enhanced survival probability (Larrea & Werner 2010). The weak effect of canopy stratification on mortality is likely an artefact of our use of binoculars, which biased our sampling effort to the low and mid-canopy. The height of the host tree, the number of branches and the abundance of large individuals in the plot (DAP ≥10 cm) were also important local-scale factors in our model that affected epiphyte mortality. These findings indicate that epiphytes on small trees with few branches tend to have a higher probability of death. At the regional scale, the actual evapotranspiration rate was the main determinant in the three categories of mortality analysed (Table 2; Fig. 2). By itself, evapotranspiration is a natural factor that has direct implications for epiphyte survival (Andrade & Nobel 1996; Nieder et al. 2000; Mondrag on, Valverde & Hernandez-Apolinar 2015). Our results bring


Determinants of vascular epiphyte mortality 847 attention to the alarming effect increased evapotranspiration due to climate change could have on tropical epiphyte assemblages (Still, Foster & Schneider 1999). However, the response of the epiphytes to the variation in evapotranspiration rates may differ between forest types. For example, the ability of many epiphyte species to resist strong droughts due to their water-saving crassulacean acid metabolism (CAM) (Winter & Smith 1996; Benzing 1998) increases in dry seasonal lowland forests and decreases in the wet and more shaded high montane forests (Zotz & Ziegler 1997; Zotz & Bader 2009). Differential physiological adaptations may define local epiphyte assemblage and function as is indicated by the high variability in mortality due to non-mechanical factors among our sites. The physiological heterogeneity among sites may also explain the weak relationship between epiphyte mortality and elevation in this study. In addition, a wide range of growth forms and species were found dead, presumably because the high tree and branch turnover must affect equally any epiphytic individual. The actual evapotranspiration was also significantly associated with the probability of epiphyte death due to mechanical factors. Increases in evapotranspiration may proportionally enhance partial or total desiccation of branches and tree trunks (Condit, Hubbell & Foster 1995; Phillips et al. 2010). Desiccation may then promote forest disturbances via fallen branches and gap formation. Since 72.2% of the epiphytes in this study died because of mechanical factors, we speculate that evapotranspiration has an indirect effect on epiphyte mortality mediated through forest dynamics and substrate instability. However, many functional characteristics of forests, such as tree wood density and growth rates, could be associated with forest disturbances (Phillips et al. 1994; ter Steege et al. 2006). For this reason, the mechanism by which evapotranspiration influences epiphyte mortality via mechanical factors remains elusive, but the results of the this study present putative relationships between forest dynamics, branchfall intensity and epiphyte mortality (Sarmento Cabral et al. 2015). Other climatic regional determinants of epiphyte mortality were temperature seasonality and the annual temperature range (Table 2). The negative relationship between these variables and the mortality indicates that epiphyte species adapted to constant temperatures could be more sensitive to sudden and unexpected changes in regular climatic conditions. We would expect that increases in temperature seasonality and annual temperature range might have stronger effects in wetter areas with low seasonality than in warmer areas with high seasonality. In climates with a high annual variation in temperature, the resident species may show a broad climatic tolerance that allows them to survive. Broader climatic tolerance may facilitate the successful survival of epiphytes in the wide range of microclimatic variations observed at different sites (Wagner, Mendieta-Leiva & Zotz 2015). Additional empirical and experimental studies are still needed to better understand the physiological response of epiphytes to changes in temperature (Zotz & Bader 2009). In conclusion, most long-term epiphyte studies have focused on the dynamics of one or a few populations

(Mondrag on 2011). To date, we are aware of only three neotropical studies that have evaluated epiphyte dynamics at the species assemblage level, and all of them were conducted in lowland forests at a local scale (Schmit-Neuerburg 2002; Laube & Zotz 2006, 2007). Although Andean forests are known to have extremely high epiphyte species richness, (K€ uper et al. 2004; Kr€ omer et al. 2005), the present study is the first to understand epiphyte dynamics at a regional scale. In Andean forests, the high rates of deforestation and landscape transformation, together with global warming (Etter & van Wyngaarden 2000; Rodrıguez Eraso, Armenteras-Pascual & Alumbreros 2013), will increase the vulnerability of epiphytes (K€ oster et al. 2009; Duque et al. 2014). Unfortunately, non-tree growth forms have been neglected in most assessments of plant dynamics despite being an important component of forest diversity (Gentry & Dodson 1987; Kelly et al. 2004; Benavides et al. 2005). We hope this study catalyses new research regarding the functional roles that non-tree growth forms play in tropical ecosystems.

Acknowledgements This study is part of the project ‘Diversity and dynamics of vascular epiphytes in Colombian Andes’ supported by COLCIENCIAS (contract 2115–2013). We would like to thank the Corporacion Autonoma Regional del Centro de Antioquia – CORANTIOQUIA, through Juan Lazaro Toro, for allowing access to the forests in their jurisdiction. Many thanks are extended to Mineros S.A., the Empresas Pecuarias del Bajo Cauca, the Fundacion Colibrı, Marleny Gil, Maya Ramirez Family, Rodrigo Celis (Hacienda San Pedro), Roman Daniel Restrepo and Maria Eugenia Sossa for the support received during the fieldwork. We are also grateful to Judith Carmona, Milena Agudelo, Samuel Monsalve, Jader Zapata, Stephany Valderrama and Sara Lopera for their assistance in the field and to Casandra Reyes-Garcia, Juan Benavides, Julio Betancur, Maria Claudia Diez and Glenda Mendieta-Leiva for their valuable contributions to the methodology used in this study. We thank to Area curricular en Bosques and Timothy Perez for corrections and editions of the English of this paper. Finally, we are very grateful to Gerhard Zotz and four anonymous referees for the comments made to this manuscript. The authors declare that they do not have any conflict of interest.

Data accessibility Epiphyte mortality data used in this study are archived at the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.g5510 (Zuleta et al. 2016).

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Supporting Information Additional Supporting Information may be found in the online version of this article: Figure S1. Observed epiphyte’s size versus estimated epiphyte’s size using binocular observations of 246 epiphyte individuals in the Andean mountains of Colombia (adjusted R2 = 0.75; d.f. = 244; P < 0.0001). Figure S2. Variogram analysis showing the lack of spatial autocorrelation of the residuals in each of the models for: total epiphyte mortality (a), epiphyte mortality caused by non-mechanical (b) and mechanical factors (c). Table S1. Local and regional variables considered as possible determinants of epiphyte mortality on 115 sampled host trees at 9 sites in the Colombian Andes.
