RESEARCH ARTICLE Tank bromeliad transplants as an enrichment strategy in southern Costa Rica Estefania P. Fernandez Barrancos1,2, J. Leighton Reid3, James Aronson3,4

Epiphytes represent up to 50% of all vascular in neotropical forests but they are among the slowest to recolonize regenerating ecosystems. This discrepancy underlines the need for restoration ecologists to learn how to assist the colonization of organisms in this key functional group. Transplanting tank bromeliads (i.e. bromeliads featuring overlapping leaves that form a water impounding rosette) could be a good approach in the neotropics, where abundant, fallen bromeliads can be sustainably collected from the forest floor. Moreover, tank bromeliads could accelerate restoration processes by providing relatively stable microenvironments for invertebrates, thus helping them resist severe drought and high temperatures, such as predicted in light of many climate change models. We transplanted 60 individuals of the tank bromeliad gladioliflora onto trunks and branches of comparable size and orientation on three host tree species. The study took place in three long-term restoration plantations located in a tropical premontane rainforest zone in southern Costa Rica. Transplant survivorship after 9 months varied among sites, from 65 to 95%. Transplants hosted twice as many arthropod orders as untreated control branches, and they buffered microclimates during the driest (+1.7 to 19.7% relative humidity) ∘ and warmest (−0.5to5.0 C) times of the day. Our results suggest that bromeliad transplantation is a cost-effective (circa $0.5 USD/successful transplant) strategy to assist the recovery of epiphyte diversity in forest restoration sites with minimal impact on source populations. Longer-term studies are needed to test this strategy for other epiphyte families or for mixed-taxa assemblages found on fallen branches. Key words: arthropods, bromeliads, epiphytes, forest restoration, microclimate

the increasing age of plantations (Toledo-Aceves et al. 2012), Implications for Practice and the presence of source populations such as those from • Dispersal limitations and slow colonization of vascular remnant trees, may facilitate recovery speed (Acuña-Tarazona epiphytes in regenerating forests underscore the impor- et al. 2015). Previous reports show the importance of includ- tance of assisting epiphyte colonization with restoration. ing nontree functional groups in restoration efforts because they • Transplanting bromeliads collected from the forest floor enhance functional diversity (Garcia et al. 2015). To our knowl- is a cost-effective strategy that helps overcome dispersal edge, very few studies have been conducted to address how to limitations found in young forest restoration sites. restore epiphyte communities in a cost-effective manner (Reid • Use of bromeliad transplants creates local microclimate et al. 2016). This fact underlines the need for applied research buffering, sheltering some arthropods against drought and to develop greater knowledge to assist vascular epiphyte colo- high temperatures. nization in regenerating tropical forests. In regenerating tropical forests, epiphyte colonization and seedling survival are limited by a diversity of factors, such Introduction as microclimatic conditions (Benzing 1978; Castro-Hernández Vascular epiphytes (hereafter, “epiphytes”) represent circa 9% of all vascular plants (Benzing 1990; Zotz 2013), up to 50% Author contributions: EFB, JLR, JA conceived and designed the research; EFB performed the experiments; EFB, JLR, JA analyzed and interpreted the data; EFB, in some neotropical forests (Gentry & Dodson 1987; Kelly JLR, JA wrote and edited the manuscript. et al. 1994), and they play important roles in canopy nutrient and water cycling and provisioning of food, water, and shel- 1Faculté de Sciences, Université de Montpellier, 2 Place Eugène Bataillon, 34090 Montpellier, France ter for animals (Ellwood & Foster 2004; Holwerda et al. 2010). 2Address correspondence to E. P. Fernandez Barrancos, email e.fernandezb2015@ However, in deforested landscapes and young plantations with gmail.com 3Center for Conservation and Sustainable Development, Missouri Botanical Garden, no remnant trees nearby, epiphyte communities are less abun- 4344 Shaw Boulevard., St. Louis, MO 63110, U.S.A. dant and diverse (Barthlott et al. 2001; Krömer & Gradstein 4Centre d’Ecologie Fonctionnelle et Evolutive (UMR 5175, Campus du CNRS), 1919, 2003; Köster et al. 2009), and have among the slowest col- route de Mende, 34293 Montpellier, France onization rates of all vascular plants in regenerating systems © 2016 Society for Ecological Restoration (Kanowski et al. 2003; Cascante-Marín et al. 2009; Martin et al. doi: 10.1111/rec.12463 Supporting information at: 2013; Woods & DeWalt 2013). It is important to note that http://onlinelibrary.wiley.com/doi/10.1111/rec.12463/suppinfo

Restoration Ecology 1 Restoration enrichment using bromeliad transplants et al. 1999; Toledo-Aceves & Wolf 2008; Toledo-Aceves et al. communities in natural forests (Kitching 2000; Ellwood & 2012), low probabilities of seed arrival to host trees, low rates Foster 2004; Jocque et al. 2013), we predicted that arthropod of germination (Mondragon & Calvo-Irabien 2006), structural communities within bromeliads from primary forests would characteristics of host trees, and the lack of a dense moss persist after translocation in restoration plantations. We further cover (Krömer & Gradstein 2003). Among these factors, dis- anticipated that bromeliads would buffer microclimates within persal limitation is an important barrier to epiphyte colonization them in comparison to ambient air (Scheffers et al. 2014). and recruitment, especially in fragmented landscapes (Mon- Finally, because bromeliads provide suitable germination sites dragon & Calvo-Irabien 2006; Cascante-Marín et al. 2009; and attract seed dispersers, we predicted that the vascular Reid et al. 2016). Therefore, manually transplanting epiphytes epiphyte colonization would increase in trees with transplants. could be a good strategy for vascular epiphyte reintroduction (Toledo-Aceves & Wolf 2008). Among tropical vascular epiphytes to be chosen for trans- Methods planting, tank bromeliads are a particularly suitable guild because many species in the family utilize Crassulacean acid Study Area metabolism (CAM) photosynthesis, which enhances their The study took place in three restoration plantations located drought tolerance (Martin & Siedow 1981; Martin et al. 2004; on the Pacific slope of southern Costa Rica, near theLas Bader et al. 2009). Bromeliads are also abundant on fallen Cruces Biological Station (lat 8∘44′77′′N, long 82∘58′32′′W) branches on the forest floor from which they can be collected in Coto Brus County. Sites are located in a premontane tropical with minimal impact on source populations (Mondragón rainforest zone (Holdridge et al. 1971) and range in elevation Chaparro & Ticktin 2011; Toledo-Aceves et al. 2014). In from 1,100 to 1,180 m a.s.l. Mean annual precipitation and addition, transplanting tank bromeliads could have a series of temperature are 3,500 mm and 21∘C, respectively (Holl et al. positive effects in the ecosystem under restoration. Because 2011). The sites are located within a mosaic of agricultural they impound water and rich soils inside their tanks, they and forest patches and were cultivated for ≥18 years prior to contribute to the renewal of water and soil nutrients in the restoration (Holl et al. 2011). canopy (Nadkarni & Matelson 1991; Holwerda et al. 2010). Thanks to this ability, they can also create microhabitats that serve as refugia, food sources, nesting sites, and foraging sites Experimental Site Layout and Design for invertebrates, mammals, and birds, increasing the number Sites (Julio Gonzales, Generoso, and Melissa’s Meadow, respec- of species interactions and ecosystem complexity (Nadkarni tively, abbreviated as JG, GN, and MM) were separated by & Matelson 1989; Benzing 1990; Cruz-Angón & Greenberg ≥0.8 km and were established in 2004–2006. Each site con- 2005; Angelini & Silliman 2014). Finally, thanks to their water tained a 50 × 50-m plantation, planted with four species of trees impounding rosette, tank bromeliads offer water sources and (313 seedlings per plantation) arranged in equidistant rows (Holl provide buffered microclimates (Stuntz et al. 2002; Scheffers et al. 2011). Mean canopy height in 2012 was 9 m (±2.0 SE) in et al. 2014) and could help arboreal animals resist extreme JG and GN, and 10 m (±2.0 SE) in MM, and all plantations had weather events that may become more frequent as a result of closed canopies (Zahawi et al. 2015). In two of the sites, GN anthropogenic climate change. and JG, the understory was undeveloped with very little herba- We report on a replicated experiment undertaken in southern ceous vegetation. In the third site, MM, which is located within Costa Rica where we tested the feasibility of bromeliad trans- a secondary forest fragment, the understory was slightly denser plantation in a tropical forest restoration context. We hypoth- with a higher number of developing young trees. From the four esized that transplanting bromeliads collected from the forest tree species planted in the restoration sites, namely, Erythrina floor is an efficient enrichment planting strategy to help recover poeppigiana (Walp.) O.F. Cook (Fabaceae), Terminalia amazo- arthropod diversity and abundance, and to overcome vascular nia (J.F. Gmel.) Exell (Combretaceae), Vochysia guatemalensis epiphyte dispersal limitations in restoration sites. We asked the Donn. Sm. (Vochysiaceae), and Inga edulis Mart. (Fabaceae), following questions: the three latter species were chosen for bromeliad transplanta- 1. Is transplanting bromeliads a viable restoration strategy that tion because their trunks were larger and they had easily acces- leads to a high survival rate of transplants and that helps sible horizontal branches. Mean diameter at breast height (cm) overcome dispersal limitations? across sites for I. edulis, T. amazonia,andV. guatemalensis was 2. Will transplanted bromeliads facilitate diverse arthropod 52.3 (±2.7 SE), 35.0 (±2.0 SE), and 59.0 (±2.1 SE) respectively. communities? A total of 90 trees were randomly selected across all sites (60 for 3. Will transplanted bromeliads buffer arboreal microclimates? transplants and 30 as controls, i.e. branches without transplants). 4. Will the presence of transplanted bromeliads facilitate fur- ther epiphyte colonization? Bromeliad Transplantation Based on results from previous translocation studies Bromeliads were collected from the forest floor on the trails (Pett-Ridge & Silver 2002; Scheffknecht et al. 2012), we near the Las Cruces Biological Station in both primary and predicted that survival rate of transplants would be above 80%. secondary forests. Care was taken to choose plants in healthy As tank bromeliads are recognized for hosting invertebrate condition: juveniles and plantlets, plants that had signs of

2 Restoration Ecology Restoration enrichment using bromeliad transplants herbivory, were dessicated, had no root system, or had a missing or damaged central rosette were discarded. In order to limit the presence of clonal individuals in the transplanted population, plants that were found aggregated in clumps were also avoided. Care was taken to select plants of similar size. Bromeliad height was measured by vertically positioning the plant on a flat surface and measuring the height from the base of the root system up to the highest naturally bent leaf. Mean bromeliad height at the time of transplanting was 33.7 (±1.2 SE) cm. Each individual was labeled with a metal numbered tag attached to the plant’s rosette. Bromeliads were stored in greenhouses for 1 week and watered every day to avoid desiccation until taxonomic verification was completed. A total of 103 bromeliads from six different species (Aech- mea dactylina Baker, mexicana Baker, Catopsis ses- siliflora (Ruiz & Pav.) Mez, Guzmania zahnii (Hook. f.) Mez, Tillandsia oerstediana L.B. Sm., and Werauhia gladioliflora (H. Wendl.) J.R. Grant) were collected and transplanted. Among these, W. gladioliflora was the only species with a representative number of transplanted individuals (n = 60); accordingly only this species was considered for analysis in this study. Informa- tion on the other transplanted species is provided in Table S1, Supporting Information. Bromeliads were transplanted between March and June 2015. Number of W. gladioliflora transplants per site was 19 in JG, 17 in GN, and 24 in MM sites. Each plant was attached to its selected host tree with twine made from organic fibers, taking care not to tighten too firmly, sothat bromeliads could gain volume as they grew or collected water Figure 1. Werauhia gladioliflora transplant attached to a Terminalia amazonia tree. Note that the plant was positioned in a manner intended to in their tanks (Fig. 1). Plants were transplanted at an average mimic its original position in the tree, with the best developed side of the height of 150 cm aboveground because bromeliads in the nat- root system oriented against the trunk to facilitate anchoring. ural forest were found at that height and because starting at that height wide, horizontal branches, and branch forks, were Jose, CA, U.S.A.) were placed into the second internal axil available. Bromeliads transplanted onto Vochysia guatemalen- of each bromeliad, without touching the water if there was sis were attached to vertical tree trunks because no horizontal any inside the rosette, and in ambient air on the outside of branches were accessible. All bromeliads were removed from each bromeliad’s rosette, at approximately 150 cm above the the trees at the end of the experiment. ground. Data loggers were covered with leaves to shelter them from solar radiation. Data were recorded during the dry season (February 2016), and measurements were taken for a minimum Bromeliad Survival of 2 days and a maximum of 4 days at 10-minute intervals. Bromeliads were revisited 9 months after transplant. Survival, presence of roots gripping the trunk (defined as new roots that had developed and anchored to the trunk), resprouting Effect of Transplants on Arthropod Community Metrics (development of plantlets at the base of the mother plant), and To evaluate bromeliad transplantation effects on arthropod flowering were recorded for each bromeliad. communities, arthropods were extracted from W. gladioliflora individuals and from control branches (0.5–1.0 m length), by introducing the selected branch or transplanted bromeliad inside Temperature and Humidity a plastic bag which was firmly closed and immediately taken Microclimate buffering was assessed for four transplanted to the laboratory. Branches and bromeliads were then placed individuals of Aechmea mexicana, a large species with inside Berlese funnels, taking care not to let any arthropods well-developed tanks. This species is a good proxy of escape. The Berlese funnels were then covered with metallic W. gladioliflora because both species are very similar in screens to avoid intrusion from other insects. Light bulbs (60 morphology but A. mexicana tanks are slightly larger than watt) were installed inside the funnels and switched on for 24 our study species. This allows for better microclimate data hours. Arthropods were collected at the bottom of the funnels measurement because the tank is developed enough so water inside plastic bags filled with 90% ethanol solution. Then, does not touch the data logger but still protects it against natural arthropod communities extracted from individual branches and elements (wind) that could bias the measurements. Data loggers bromeliads (hereafter referred to as “samples”) were counted (Maxim Hygrochron, model: DS1923, Maxim Integrated, San and identified using the taxonomic key of Delvare and Aberlenc

Restoration Ecology 3 Restoration enrichment using bromeliad transplants

(1989). Identifications were performed to order for insects and other invertebrates, class (Diplopoda, Chilopoda), or subclass (Acarina), depending on the identification resources available, but for convenience we will refer to all these taxa as “orders” (Table S2).

Epiphyte Recruitment Facilitation To assess whether transplanted bromeliads facilitated additional epiphyte recruitment, nontransplanted epiphytes were surveyed twice: once at the time of transplantation and again after 9 months. Surveys were performed on each side of each host tree, up to 4 m aboveground level. Epiphytes were identified in the field to the level of family.

Statistical Analyses Thermal microclimate buffering was estimated by subtracting daily maximum temperatures inside transplanted bromeliads from daily maximum ambient temperatures. The same approach was used to estimate humidity buffering (Table S3). Local Figure 2. Survival of Werauhia gladioliflora transplants in three temperature and humidity data were continuous and unbounded; restoration plantations in southern Costa Rica. Site abbreviations: GN, thus it was considered legitimate to assume they followed a Generoso; JG, Julio Gonzales; MM, Melissa’s Meadow. normal distribution. Paired t tests were carried out to assess whether temperature and humidity were significantly different trunks/branches with their roots, 5% (±3.4 SE) produced between ambient air and air inside the bromeliads, and whether flowers and seeds, and 11%± ( 10.5 SE) resprouted (i.e. pro- buffering effects were significantly greater than zero. duced new plantlets at their bases), with the latter variable being Arthropod abundance, order richness, and order diversity observed at only one site (Table S4). (Simpson’s index) were calculated for transplanted bromeli- ads and control branches. Because were very abundant Microclimate Buffering in some samples, they were excluded from abundance and diversity calculations (which they strongly impacted), but were Maximum temperature was lower inside bromeliads com- retained for richness, as they were often the only representatives pared to the ambient air outside the rosette. Results from of Hymenoptera. Differences in arthropod community metrics one-sided t tests showed significant difference between daily < −3 were estimated between branches with W. gladioliflora trans- maximum temperature (p 5.0 × 10 , t = 4.1) in ambient air 𝜇 ∘ 𝜇 ∘ plants and branches without transplants (controls) using gener- ( = 25.0 C ± 0.5 SE) and bromeliads ( = 23.3 C ± 0.5 SE). alized linear mixed effects regression (GLMER) with a random One-sided t tests showed that daily maximum temperature site effect. Poisson error distribution was used for abundance in ambient air was significantly greater relative to bromeli- < −3 and richness and binomial distribution for diversity. To assess ads’ interior (p 1.0 × 10 , t = 4.1). Minimum humidity was overall model fit (pseudo-R2), deviance in fitted models was greater inside transplanted bromeliads in comparison to the compared to deviance in null (i.e. random effects) models. ambient air nearby. Two-sided t tests performed on daily min- To assess the effect of transplanted bromeliads on additional imum humidity showed that this variable was significantly < −05 epiphyte recruitment, a Wilcoxon signed ranks paired t test different between the two treatments (p 3.2 × 10 , t = 6.7), was used to compare recruit abundance between trees with with a mean daily relative humidity (%) of 86.7 (±6.3 SE) transplants and trees without transplants, both at the time of inside bromeliads and 71.6 (±5.0 SE) in ambient air. One-sided transplantation and after 9 months. t tests showed that daily minimum humidity was significantly < −05 Statistical analyses were performed using the package “lme4” lower in ambient air compared to bromeliads (p 1.6 × 10 , (Bates et al. 2015) in R version 3.2.3 (R Development Core t = 4.1; Fig. 3). Buffering effects were also significantly greater 𝜇 ∘ < −3 Team, 2008). Data will be made available (pending publication) than zero, for temperature ( = 1.7 C ± 0.0 SE, p 1 × 10 ) 𝜇 < −05 at https://merritt.cdlib.org/m/ucsc_lib_hollzahawi. and humidity ( = 15.1% ± 0.0 SE, p 1.6 × 10 ).

Results Arthropod Habitat Provisioning Arthropod communities in transplanted bromeliads were Transplant Survival seven times as abundant (𝜒2 = 1218.2, p < 2.2 × 10−16 Rate of survival after 9 months varied among sites (65–95%), pseudo-R2 = 0.7), and two times as rich (𝜒2 = 35.8, with a mean survivorship of 75% (±9.7 SE; Fig. 2). Among p = 2.1 × 10−09 pseudo-R2 = 0.9) as untreated control branches surviving individuals, 59% (±5.0 SE) gripped host tree after 9 months (Figs. 4 & S1). Order diversity was significantly

4 Restoration Ecology Restoration enrichment using bromeliad transplants

Figure 3. Daily temperature (left) and humidity (right) recorded by data loggers over a 3-day period in an Aechmea mexicana transplant.

epiphyte abundance did not increase in trees with (p = 0.9) or without (p = 0.3) transplanted bromeliads.

Costs Untrained field assistants were paid a monthly salary of 690.0 USD (3.6 USD per hour), that is the legal minimum salary in Costa Rica for a nonqualified worker in the silvicultural sector, plus social welfare charges paid by employers such as health insurance and additional allowances. Approximately 6 hours were needed for one person to collect the 60 bromeliads from the forest floor, bring the transplants to the sites, and transplant them. This resulted in a final cost of 0.5 USD per successful transplant (45 transplants survived out of a total of 60 transplanted bromeliads).

Discussion Vascular epiphytes are fundamental elements of tropical ecosys- tems but often recolonize secondary forests slowly, suggest- ing a role for ecological restoration. We observed acceptable (75%) survivorship and establishment in bromeliads from Wer- Figure 4. Arthropod abundance in control branches and Werauhia auhia gladioliflora translocated from secondary and old-growth gladioliflora transplants in each site 9 months after transplantation. Site forests into three young restoration plantations. Moreover, trans- abbreviations: GN, Generoso; JG, Julio Gonzales; MM, Melissa’s planted bromeliads contributed to ecosystem function and biodi- Meadow. Asterisks indicate a significant increase in arthropod abundance in branches with transplants compared to control branches (***p < 0.001; versity by buffering against temperature and humidity extremes, **p < 0.01). Error bars correspond to ± SE. and by providing microhabitats for diverse invertebrate com- munities. In sum, our results, even though restricted to the 9 months of data collection, suggest that bromeliad transplanta- higher in branches with bromeliads compared to branches tion is an effective epiphyte enrichment strategy for neotropical 𝜒2 2 without them ( = 10.1, p = 0.01, pseudo-R = 0.9; Fig. S2; forest restoration. for more information on arthropod community structure across sites and statistical analyses see Tables S5 & S6). Transplant Survival Bromeliad survivorship in our study was comparable to previous Epiphyte Recruitment Facilitation translocation experiments in coffee plantations (Scheffknecht Contrary to our expectations, transplanted bromeliads did not et al. 2012; 70% survival after 7 months in Central Veracruz, facilitate additional epiphyte recruitment. Nontransplanted Mexico) and natural forests (Pett-Ridge & Silver 2002; 97%

Restoration Ecology 5 Restoration enrichment using bromeliad transplants survival after 6 months at the Luquillo Experimental Forest in subject to higher temperatures and vapor pressure deficits than Puerto Rico). Mean survival in our study species was 75%, and intact forests because of their less complex and more open survival across sites ranged from 65 to 95%. Furthermore, we structure (Holl et al. 2000; Barthlott et al. 2001; Krömer & observed resprouting at one site in 32% of surviving plants and Gradstein 2003; Köster et al. 2009; Larrea & Werner 2010). flowers and/or seed in 16% surviving plants suggesting that These results are limited by our small sample and the short restored forests may provide suitable habitat for translocated period during which recordings were carried out but suggest bromeliads. While our transplants were carried out at 150 cm that the “air conditioning” role of tank epiphytes might be even aboveground, it is important to note that transplanting epiphytes greater in restoration sites than in old secondary and old-growth in the canopy could enhance seed production and dispersal from forests. Previous studies have shown that when abundant, epi- transplants for additional epiphyte recruitment. When access phyte loaded branches can have an effect on the nearby ambi- to the canopy is possible, transplanting epiphytes higher on ent air (Freiberg 2001; Stuntz et al. 2002). This effect was not the trees is therefore recommended when testing applying this assessed in this study because natural epiphyte density was very strategy. low in our plantations, transplants were scattered across each In a recent study, Reid et al. (2016) suggested that site (more than 200 cm separation between trees holding a trans- angiosperm epiphyte colonization in restored forests was plant), and individual bromeliads were transplanted into single contingent on landscape context (forest cover and elevation), trees making it difficult to evaluate the effect of the transplanted presumably because restored sites far from propagule sources population on local microclimate. could not be reached. Our findings support the notion that transplantation is an effective means for overcoming epiphyte dispersal limitation. Moreover, our data suggest that bromeliad Provisioning of Arthropod Habitat transplantation can be carried out relatively inexpensively and Transplanted bromeliads more than doubled abundance and with minimal impact on source populations if fallen plants are species richness of arthropods compared to untreated tree used. Bromeliad population survival and demography display branches, indicating that transplanted bromeliads provide refu- important temporal variation because they depend on a diverse gia in restoration plantations. The arthropod abundance ratio set of abiotic (rainfall or the length of the drought season) and between bromeliads and control branches, ants included, was biotic (competition and/or facilitation by nearby epiphytes, similar to that estimated by Angelini and Silliman (2014), who branch falling and bark flaking) factors. We acknowledge that found 20 times more arthropods on tree limbs with Tilland- our results are limited to the 9-month period within which the sia usneoides relative to bare limbs; in our study, we found up experiment took place and that longer-term studies are needed to 23 times greater abundance in bromeliads than in control to confirm our preliminary trials and provide more insight branches. Our study also revealed that there is suitable habi- into long-term effects of transplantings aimed at reestablish- tat for bromeliad arthropod communities in the restoration sites ing viable epiphyte populations and ameliorating microsite where we worked. This finding complements previous studies conditions for arthopods. (Cruz-Angón et al. 2009; Hénaut et al. 2014) that underscore the importance of epiphytic bromeliads in supporting diverse invertebrate communities which in turn play an essential role Microclimate Buffering in the renewal of nutrients in forest canopies (Angelini & Sil- Epiphytes have been called the “air-conditioners” (Stuntz et al. liman 2014) and serve as food for birds and arboreal mammals 2002) of the forest canopy because they buffer local micro- (Nadkarni & Matelson 1989; Benzing 1990). climates against temperature and humidity extremes. Although previous studies have documented this effect in natural com- munities (Freiberg 2001; Stuntz et al. 2002; Cardelus & Chaz- Epiphyte Recruitment Facilitation don 2005; Angelini & Silliman 2014; Scheffers et al. 2014), Transplanted bromeliads could accelerate additional epiphyte our results extend the discourse on microclimate buffering to recruitment by attracting seed dispersal or facilitating seedling arboreal habitats in forests undergoing ecological restoration. germination; however, over the relatively short period of this While we observed a buffering effect that ranged between 0.5 experiment, we were not able to detect an increase in epiphyte and 2.0∘C, the above-mentioned studies indicated a slightly colonization due to transplanted bromeliads. This is not surpris- lower buffering effect, ranging from 0.5 to 1.0∘C. This could be ing given that the interval between the two surveys was just 9 explained by three factors: (1) a difference in the method used months and also that we worked in the long interval prior to for measuring these parameters; we took measurements every the start of the rainy season, in which dispersed seeds are most 10 minutes, for a minimum of 48 hours, as compared to Stuntz likely to germinate. Anecdotally, 13 epiphyte plantlets were et al. (2002) who measured these parameters only at midday; found inside the rosettes and root systems of eight transplanted (2) differences in the architecture and size of the studied plants; bromeliads. Even though this number is small, it suggests that in contrast to Angelini and Silliman (2014) who took measure- inside transplanted tank bromeliads there may be favorable ments inside bromeliad “festoons” (of Tillandsia usneiodes), conditions for germination, potentially because trapped seeds we measured microclimatic conditions inside tank bromeliads; are protected from predation and/or environmental exposure. and (3) unlike the above-cited studies, we estimated bromeliad This anecdote tends to agree with previous reports on the role buffering effects within tree plantations, which are probably of bromeliads as nurse-plants for seed germination (Fialho &

6 Restoration Ecology Restoration enrichment using bromeliad transplants

Furtado 1993; Tsuda & Castellani 2015; but see Brancalion Castro-Hernández JC, Wolf JHD, García-Franco JG, González-Espinosa M et al. 2009). (1999) The influence of humidity, nutrients and light on the establishment Slow epiphyte recovery requires that we identify and develop of the epiphytic bromeliad Tillandsia guatemalensis in the highlands of cost-effective techniques that will speed and enhance suc- Chiapas, Mexico. Revista de Biología Tropical 47:763–773 Cruz-Angón A, Greenberg R (2005) Are epiphytes important for birds in coffee cess rate of colonization for this highly important functional plantations? An experimental assessment. Journal of Applied Ecology group of tropical forest plants. Our results show that trans- 42:150–159 planting bromeliads can be a simple, nondestructive approach Cruz-Angón A, Baena ML, Greenberg R (2009) The contribution of epiphytes to that helps overcome epiphyte dispersal limitations and accel- the abundance and species richness of canopy insects in a Mexican coffee erate biodiversity recovery. The effectiveness of this strategy plantation. Journal of Tropical Ecology 25:453–463 will ultimately depend on the survival of transplants and on Delvare G, Aberlenc H-P (1989) Les insectes d’Afrique et d’Amérique tropicale: their reproductive success and establishment on the long term. Clés pour la reconnaissance des familles. Quae Press, Versailles, France Further research is needed to test the approach described here Ellwood MDF, Foster WA (2004) Doubling the estimate of invertebrate biomass in a rainforest canopy. Nature 429:549–551 using a larger number of epiphytes, additional families, or even Fialho R, Furtado A (1993) Germination of Erythroxylum-Ovalifolium (Ery- entire epiphyte communities as “inocula” to facilitate further throxylaceae). Seeds within the terrestrial bromeliad Neoregelia cruenta. epiphyte colonization. Biotropica 25:359–362 Freiberg M (2001) The influence of epiphyte cover on branch temperature in a tropical tree. Plant Ecology 153:241–250 Acknowledgments Garcia LC, Cianciaruso MV, Ribeiro DB, dos Santos FAM, Rodrigues RR (2015) Flower functional trait responses to restoration time. Applied Vegetation We thank K. Holl and R. Zahawi for the use of their long-term Science 18:402–412 restoration plots, R. Zahawi and D. McKey for guidance, F.O. Gentry A, Dodson C (1987) Diversity and biogeography of neotropical vascular Brenes for help with identification, A. Matarrita and D. Janas epiphytes. Annals of the Missouri Botanical Garden 74:205–233 for field assistance, and Las Cruces Biological Station staff Hénaut Y, Corbara B, Pélozuelo L, Azémar F, Céréghino R, Herault B, Dejean A for logistical support. We are grateful to the Organization for (2014) A tank bromeliad favors presence in a neotropical inundated Tropical Studies, the Center for Conservation and Sustainable forest. PLoS One 9:e114592 Development of the Missouri Botanical Garden, and the Cen- Holdridge LR, Grenke WC, Hatheway WH, Liang T, Tosi JA (1971) Forest tre d’Ecologie Fonctionnelle et Evolutive (CNRS) for fund- environments in tropical life zones: a pilot study. Pergamon Press, Oxford, U.K. ing. We also warmly thank Dr. J. Parotta and two anonymous Holl KD, Loik ME, Lin EHV, Samuels IA (2000) Tropical montane forest reviewers for very helpful comments on an earlier version of restoration in Costa Rica: overcoming barriers to dispersal and establish- the manuscript. ment. 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Restoration Ecology 7 Restoration enrichment using bromeliad transplants

Martin PA, Newton AC, Bullock JM (2013) Carbon pools recover more quickly Tillandsia species in the cloud-forest canopy. Journal of Tropical than plant biodiversity in tropical secondary forests. Proceedings of the Ecology 28:423–426 Royal Society Biological Sciences 280:20132236–20132236 Toledo-Aceves T, García-Franco JG, López-Barrera F (2014) Bromeliad rain: an Mondragon D, Calvo-Irabien LM (2006) Seed dispersal and germination of the opportunity for cloud forest management. Forest Ecology and Management epiphyte Tillandsia brachycaulos (Bromeliaceae) in a tropical dry forest, 329:129–136 Mexico. The Southwestern Naturalist 51:462–470 Tsuda ÉT, Castellani TT (2015) friburgensis: a natural trap or a nurse Mondragón Chaparro D, Ticktin T (2011) Demographic effects of harvesting epi- plant in coastal sand dunes? Austral Ecology 41:273–281 phytic bromeliads and an alternative approach to collection. Conservation Woods CL, DeWalt SJ (2013) The conservation value of secondary forests for Biology 25:797–807 vascular epiphytes in central Panama. Biotropica 45:119–127 Nadkarni NM, Matelson TJ (1989) Bird use of epiphyte resources in neotropical Zahawi RA, Dandois JP, Holl KD, Nadwodny D, Reid JL, Ellis EC (2015) Using trees. The Condor 91:891–907 lightweight unmanned aerial vehicles to monitor tropical forest recovery. Nadkarni NM, Matelson TJ (1991) Fine litter dynamics within the tree canopy Biological Conservation 186:287–295 of a tropical cloud forest. Ecology 72:2071–2082 Zotz G (2013) The systematic distribution of vascular epiphytes a critical update. Pett-Ridge J, Silver WL (2002) Survival, growth, and ecosystem dynamics of Botanical Journal of the Linnean Society 171:453–481 displaced bromeliads in a montane tropical forest. Biotropica 34:211–224 Reid JL, Chaves-Fallas JM, Holl KD, Zahawi RA (2016) Tropical forest restora- tion enriches vascular epiphyte recovery. Applied Vegetation Science Supporting Information 19:508–517 The following information may be found in the online version of this article: R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Table S1. Percent survival of each bromeliad species across the three restoration sites Scheffers BR, Evans TA, Williams SE, Edwards DP (2014) Microhabitats in the and number of bromeliads transplanted in each site (GN, Generoso; JG, Julio Gonzales; MM, Melissa’s Meadow). tropics buffer temperature in a globally coherent manner. Biology Letters Table S2. Mean order abundance of invertebrates inside three sampled bromeliad 10:20140819 species and control branches 9 months after transplantation. Scheffknecht S, Winkler M, Mata-Rosas M, Hietz P (2012) Survival and growth Table S3. Daily maximum temperature (∘C) and minimum humidity (%) recorded of juvenile bromeliads in coffee plantations and forests in central Veracruz, for each monitored bromeliad and for the corresponding ambient air outside each Mexico. Biotropica 44:41–349 bromeliad. Stuntz S, Simon U, Zotz G (2002) Rainforest air-conditioning: the moderating Table S4. Percent survival, flowering, and resprouting of Werauhia gladioliflora influence of epiphytes on the microclimate in tropical tree crowns. Inter- transplants across three restoration sites in southern Costa Rica. national Journal of Biometeorology 46:53–59 Table S5. Arthropod community structure in transplanted Werauhia gladioliflora and Toledo-Aceves T, Wolf JHD (2008) Germination and establishment of Tillandsia control branches. Table S6. GLMER results for the effect of branches with transplants versus branches eizii (Bromeliaceae) in the canopy of an oak forest in Chiapas, Mexico. without transplants on arthropod community metrics. Biotropica 40:246–250 Figure S1. Arthropod richness in control branches and Werauhia gladioliflora trans- Toledo-Aceves T, García-Franco JG, Lozada SL, Mateos MLL, MacMil- plants in each site 9 months after transplantation. lan K (2012) Germination and seedling survivorship of three Figure S2. Arthropod diversity in control branches and Werauhia gladioliflora transplants in each site 9 months after transplantation.

Coordinating Editor: John Parrotta Received: 26 April, 2016; First decision: 25 May, 2016; Revised: 7 October, 2016; Accepted: 7 October, 2016

8 Restoration Ecology